Re-visiting the Rhizosphere Eco-system for Agricultural Sustainability (Rhizosphere Biology) 9811941009, 9789811941009

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Rhizosphere Biology

Udai B. Singh Jai P. Rai Anil K. Sharma   Editors

Re-visiting the Rhizosphere Eco-system for Agricultural Sustainability

Rhizosphere Biology Series Editor Anil Kumar Sharma, Biological Sciences, CBSH, G.B. Pant University of Agriculture & Technology, Pantnagar, Uttarakhand, India

The Series Rhizosphere Biology, emphasizes on the different aspects of Rhizosphere. Major increase in agricultural productivity, to meet growing food demands of human population is imperative, to survive in the future. Along with methods of crop improvement, an understanding of the rhizosphere biology, and the ways to manipulate it, could be an innovative strategy to deal with this demand of increasing productivity. This Series would provide comprehensive information for researchers, and encompass all aspects in field of rhizosphere biology. It would comprise of topics ranging from the classical studies to the most advanced application being done in the field. Rhizoshpere is a dynamic environment, and a series of processes take place to create a congenial environment for plant to grow and survive. There are factors which might hamper the growth of plants, resulting in productivity loss, but, the mechanisms are not very clear. Understanding the rhizosphere is needed, in order to create opportunities for researchers to come up with robust strategies to exploit the rhizosphere for sustainable agriculture. There are titles already available in the market in the broad area of rhizosphere biology, but there is a major lack of information as to the functions and future applications of this field. These titles have not given all the up-to-date information required by the today’s researchers and therefore, this Series aims to fill out those gaps.

Udai B. Singh • Jai P. Rai • Anil K. Sharma Editors

Re-visiting the Rhizosphere Eco-system for Agricultural Sustainability

Editors Udai B. Singh Plant-Microbe Interaction & Rhizosphere Biology Lab, ICAR-National Bureau of Agriculturally Important Microorganisms Kushmaur, Uttar Pradesh, India

Jai P. Rai Department of Mycology and Plant Pathology (BHU-KVK) Institute of Agricultural Sciences, Banaras Hindu University, RG South Campus Mirzapur, Uttar Pradesh, India

Anil K. Sharma Department of Biological Sciences G.B. Pant University of Agriculture and Technology Pantnagar, Uttarakhand, India

ISSN 2523-8442 ISSN 2523-8450 (electronic) Rhizosphere Biology ISBN 978-981-19-4100-9 ISBN 978-981-19-4101-6 (eBook) https://doi.org/10.1007/978-981-19-4101-6 # The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2022 This work is subject to copyright. All rights are solely and exclusively licensed by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors, and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, expressed or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. This Springer imprint is published by the registered company Springer Nature Singapore Pte Ltd. The registered company address is: 152 Beach Road, #21-01/04 Gateway East, Singapore 189721, Singapore

Preface

Plants create a dynamic micro-biosphere in the soil, around the roots, called as “rhizosphere,” which harbors a number of microorganisms for sustaining their growth and development. It renders a small zone around the roots and is one of the most energy-rich habitats on Earth. Its micro-environment is contrastingly different from that of a non-rhizosphere soil. Consequently, rhizosphere is the central player in a complex food web in which numerous members of flora and fauna profusely take advantage of the plant’s resources. Soils with diverse and multitrait microbial communities are considered healthy and are crucial for enhancing crop productivity. The rhizosphere, one of the most dynamic interfaces on Earth, contains up to 1011 microbial cells per gram of soil representing over 30,000 bacterial species. In the last decades, rhizosphere biology has gained attention due to unraveling of new mechanisms, processes, and molecules in the rhizosphere that contribute to the enhancement of plant productivity. The rhizospheric microbes and associated processes are being utilized for harnessing the potential of soils for their effective and sustainable functioning in the agro-ecosystems. This zone contains sloughed-off root, root exudates, mucilage, and gases. The gases released from roots in the soil dissipate to comparatively longer distances leading to the extended size of the rhizospheric zone up to many centimeters. The rhizosphere is of paramount importance to ecosystem services, namely carbon and water cycling, nutrient trapping/cycling or mobilization, carbon uptake and storage, etc. Plant rhizosphere is the battlefield for a variety of beneficial and harmful organisms. Besides insect herbivores and plant pathogens in the rhizosphere, plants also nurture a vast community of commensal and mutualistic flora and fauna that provide the plant with indispensable services like nitrogen fixation, protection from pathogens, enhanced mineral uptake, and growth promotion. The significance of plant–microbe interactions in the rhizosphere ecosystem is enormous for agricultural sustainability. These interactions may be positive such as the interaction of the plants with the beneficial soil microorganisms for inducing the plant growth, conferring abiotic and biotic stress tolerance, and modulating several pathways of the plants for the proper establishment and revitalization of degraded and contaminated soils or negative likes the host–pathogen interactions leading to disease development in the plants. Moreover, below-ground communication among the plant, soil insects, and microbes plays an important role in the rhizosphere ecosystem functioning and modulates v

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the physio-biochemical pathways leading to better plant growth and productivity under biotic and abiotic stresses. Further, plant secretome shapes the rhizospheric microbial community by recruiting the specific microflora around the root system and interacting with them. However, rhizospheric interactions are quite complex and dynamic and are rather difficult to elucidate as they take place under different circumstances and at different interfaces in and around the rhizosphere. It is evident that recent technological advancements play a crucial role not only in the elucidation of but also in large-scale exploitation of the rhizospheric interactions for enhancing the agro-ecosystems’ resilience to abiotic and biotic stresses and thus maximizing the sustainable food production under such adverse conditions. In this context, the proposed book Re-visiting the Rhizosphere Ecosystem for Agricultural Sustainability is an opportune contribution to the topical information on plant– microbe interactions offering a great scope for harnessing the beneficial interactions for agricultural sustainability. This book encompasses and addresses various issues of plant and soil–microbe interrelationship that are to be modulated either by resident microbes or by their external application. The book discusses rhizospheric microbes and their role in modulating functions of soil and crop plants in detail. It also provides information on microbiomes in the rhizosphere, cross-talk among microorganisms and plants, functions of soil microflora, regulations relating to biofertilizers and biostimulants, and products and technologies of microbes in the soil. It also covers conventional and modern aspects of rhizosphere biology such as rhizosphere microbes as biofertilizers, biostimulators and biofortifiers, microbial signaling in the rhizosphere, and recent tools in deciphering rhizomicrobiome. The book provides the latest understanding of rhizosphere microorganisms for enhanced soil and plant functions, thereby improving agricultural sustainability and food and nutritional security. The aim of the book is to compile high-quality reviews and research articles offering new insight into rhizosphere interactions, ecology and function of the rhizosphere, harnessing plant–microbe interactions for biotic and abiotic stress tolerance, etc. By bringing all these areas together within the ambit of this special book, we hope to build cohesion between conventional and most modern approaches of science to design the future path for Agricultural Sustainability. This book addresses various issues of phytobiome and rhizomicrobiome in detail. The book covers (1) the composition, structure, and function of the rhizosphere; (2) recruitment of microorganisms in the rhizosphere; (3) rhizo-deposits and their role in rhizosphere interactions among the plant, microbe, and other ecological components; (4) understanding the below-ground communication in the rhizosphere for better plant growth; (5) omics approaches to unravel the rhizosphere interactions and functions; (6) rhizosphere engineering for ecosystem restoration and sustainable crop production in degraded lands; (7) rhizosphere engineering for systemic resistance/tolerance to biotic and abiotic stresses; and (8) microbial inventerization for sustainable crop production. We expect that the book would be useful for students, agricultural scientists, biotechnologists, plant pathologists, mycologists, and microbiologists, the farming community, scientists of R&D organizations, as well as the teaching community, researchers, and policymakers to understand the roles of rhizospheric

Preface

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microorganisms and associated ecosystem in sustainable agriculture and provide directions for the future course of action. Kushmaur, Uttar Pradesh, India Mirzapur, Uttar Pradesh, India Pantnagar, Uttarakhand, India

Udai B. Singh Jai P. Rai Anil K. Sharma

Contents

1

Evolution of the Knowledge and Practice of Endophytic Microorganisms for Enhanced Agricultural Benefit and Environmental Sustainability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Gary E. Harman

2

Mycorrhizosphere Revisited: Multitrophic Interactions . . . . . . . . . T. Muthukumar, C. S. Sumathi, V. Rajeshkannan, and D. J. Bagyaraj

3

Conservation Strategies for Rhizobiome in Sustainable Agriculture . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Md. Mahtab Rashid, Basavaraj Teli, Gagan Kumar, Prerna Dobhal, Dhuni Lal Yadav, Saroj Belbase, Jai Singh Patel, Sudheer Kumar Yadav, and Ankita Sarkar

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Exploring the Rhizosphere Microbiome for Sustainable Agriculture Production . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Anamika Dubey and Ashwani Kumar From Rhizosphere to Endosphere: Bacterial-Plant Symbiosis and Its Impact on Sustainable Agriculture . . . . . . . . . . . . . . . . . . . Gaurav Pal, Kanchan Kumar, Anand Verma, and Satish Kumar Verma

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37

63

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6

Arbuscular Mycorrhizal Fungal Symbiosis for Mutual Benefit: More Than Expectation . . . . . . . . . . . . . . . . . . . . . . . . . . . 105 Harsh V. Singh, Udai B. Singh, Pramod K. Sahu, Deepti Malviya, Shailendra Singh, and Anil K. Saxena

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Rhizodeposits: An Essential Component for Microbial Interactions in Rhizosphere . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 129 Madhurankhi Goswami and Suresh Deka

8

Rhizospheric Microbial Diversity: Organic Versus Inorganic Farming Systems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 153 Asha Sahu, Asit Mandal, Anita Tilwari, Nisha Sahu, Poonam Sharma, and Namrata Pal ix

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Rhizomicrobes: The Underground Life for Sustainable Agriculture . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 167 Tanwi Sharma, Manoj K. Dhar, and Sanjana Kaul

10

Synthetic Biology Tools in Cyanobacterial Biotechnology: Recent Developments and Opportunities . . . . . . . . . . . . . . . . . . . . . 181 Krishna Kumar Rai, Ruchi Rai, Shilpi Singh, and L. C. Rai

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The Potential of Rhizobacteria for Plant Growth and Stress Adaptation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 205 Gustavo Ravelo-Ortega and José López-Bucio

12

Mycoremediation: An Emerging Technology for Mitigating Environmental Contaminants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 225 Manisha Mishra and Deepa Srivastava

13

Exploration of Plant Growth-Promoting Rhizobacteria (PGPR) for Improving Productivity and Soil Fertility Under Sustainable Agricultural Practices . . . . . . . . . . . . . . . . . . . . 245 Gowardhan Kumar Chouhan, Saurabh Singh, Arpan Mukherjee, Anand Kumar Gaurav, Ayush Lepcha, Sudeepa Kumari, and Jay Prakash Verma

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Rhizosphere Engineering for Systemic Resistance/Tolerance to Biotic and Abiotic Stress . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 271 Jyotsana Tilgam, N. Sreeshma, Parichita Priyadarshini, R. K. Bhavyasree, Sharani Choudhury, Alka Bharati, and Mushineni Ashajyothi

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Understanding the Microbiome Interactions Across the Cropping System . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 301 C. M. Mehta, Raghavendra Reddy Manda, Ravindra Kumar, Vinit Pratap Singh, Udai B. Singh, Meenakshi Rana, and Seweta Srivastava

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Role of Rhizosphere Microorganisms in Endorsing Overall Plant Growth and Development . . . . . . . . . . . . . . . . . . . . . . . . . . . 323 Soma Gupta, Udai B. Singh, Ashutosh Kumar, Vinita Ramtekey, Deepanshu Jayaswal, Arvind Nath Singh, Paramanand Sahni, and Sanjay Kumar

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Rhizospheric Microbial Community as Drivers of Soil Ecosystem: Interactive Microbial Communication and Its Impact on Plants . . . 355 Ved Prakash, Sneha Tripathi, Samarth Sharma, Shweta Rana, Vivek Kumar, Durgesh Kumar Tripathi, and Shivesh Sharma

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Rhizospheric Microbes and Plant Health . . . . . . . . . . . . . . . . . . . . . 373 Jharjhari Chakma, Satyendra Pratap Singh, and Dawa Dolma Bhutia

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Omics Approaches to Unravel the Features of Rhizospheric Microbiome . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 391 Sandeep Kumar Singh, Subhesh Saurabh Jha, and Prem Pratap Singh

20

Rhizo-Deposit and Their Role in Rhizosphere Interactions Among the Plant, Microbe and Other Ecological Components for Crop Management . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 403 Ramji Singh, Ajay Tomar, H. S. Viswanath, Durga Prasad, and Sachin Kumar

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Effects of Irrigation with Municipal Wastewater on the Microbiome of the Rhizosphere of Agricultural Lands . . . . . . . . . . 427 Theodore C. Crusberg

22

Plant–Rhizospheric Microbe Interactions: Enhancing Plant Growth and Improving Soil Biota . . . . . . . . . . . . . . . . . . . . . 445 R. K. Mishra, Utkarsh Singh Rathore, Sonika Pandey, Monika Mishra, Nitish Sharma, Sandeep Kumar, and Kulbhushan Mani Tripathi

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Microbes-Mediated Rhizospheric Engineering for Salinity Stress Mitigation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 461 Vinita Ramtekey, Ashutosh Kumar, Akhilendra Pratap Bharati, Sunita Kumari, Paramanand Sahni, Soma Gupta, Udai B. Singh, Govind Pal, Arvind Nath Singh, Gopi Kishan, and Sanjay Kumar

24

Metatranscriptomics of Plant Rhizosphere: A Promising Tool to Decipher the Role of Microorganisms in Plant Growth and Development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 491 K. Pandiyan, Prity Kushwaha, Ruchi Srivastava, and Prem Lal Kashyap

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Rhizospheric Engineering for Sustainable Production of Horticultural Crops . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 511 Sarita Devi and Poonam Kumari

Editors and Contributors

About the Editors Udai B. Singh presently working as a Scientist (Senior Scale) in the Plant-Microbe Interaction and Rhizosphere Biology Lab, ICAR-National Bureau of Agriculturally Important Microorganisms, Kushmaur, Maunath Bhanjan, Uttar Pradesh, India. His specialized areas are: plant–microbe interactions in the rhizosphere with special reference to biotic and abiotic stress management/molecular biology/biotechnology/plant pathology. As an active researcher, Dr Singh has published many research and review articles in the journals of national and international reputes and book chapters in edited books. He has developed some microbial-based bioformulations/ technologies for sustainable crop production. His team has developed databases and web-based portals for public use. His developed portal (www.mgrportal.org.in) has been awarded copyright. Dr Singh has been awarded “DST Young Scientist” under Fast-Track Scheme, “Young Scientist award” of RASSA, New Delhi, Bharat Shiksha Ratan Award, K.P.V. Menon and Prof. K.S. Bilgrami Best Poster Award for the Year 2018 by Indian Phytopathological Society, New Delhi, and Indian Society of Mycology and Plant Pathology, Udaipur. Plant-Microbe Interaction and Rhizosphere Biology Lab, ICAR-National Bureau of Agriculturally Important Microorganisms, Kushmaur, Maunath Bhanjan, Uttar Pradesh, India Jai P. Rai is presently working as Associate Professor (Plant Protection), Department of Mycology and Plant Pathology (BHU-KVK), Institute of Agricultural Sciences, Banaras Hindu University, RG South Campus, Barkachha Mirzapur, Uttar Pradesh, India. He has an extensive experience in teaching, research, and extension for more than two decades. Dr Rai is a prolific writer and has authored a number of research and review papers of international acclaim, books, book chapters, popular articles, and a laboratory manual for students of Plant Pathology. Apart from authorship, he is also on the panel of reviewers of several international journals and publication houses and has conducted reviews for more than a hundred articles. Dr Rai is also a proud recipient of several awards. The Rajbhasha Award for the year 2013 was conferred to him by the then President of India, Hon’ble Shri Pranab Mukherjee for original writing. Dr Rai has also been a recipient of Award of xiii

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Editors and Contributors

Excellence for Energy Awareness in Agriculture by IIT, BHU, and has been declared Scientist of the Year 2015 by the Scientific Advance Agriculture Research Society for his contribution to the field of Agricultural Sciences. Department of Mycology and Plant Pathology (BHU-KVK), Institute of Agricultural Sciences, Banaras Hindu University, Barkachha, Mirzapur, Uttar Pradesh, India Anil K. Sharma is a Professor at the Department of Biological Sciences, CBSH G.B. Pant University of Agriculture and Technology, Pantnagar. He was a Visiting Scientist at the University of Basel, Switzerland, from July 2003–November 2003 and at the University of Helsinki, Finland, in 2013. He completed his post-doctoral studies at GSU, Louisiana, USA, and he has extensive research and teaching experience. He is a reviewer for DBT, DST, and MOEF projects, and journals such as the Biocontrol Journal, International Journal of Agriculture, and Microbiology. He holds three patents in the field of plant biology and microbiology and has received a number of prestigious grants. His laboratory is involved in various international collaborations, and he has published more than 84 research articles, 32 review articles, and two books with renowned publishers. He has presented his research on several internationally acclaimed platforms. Department of Biological Sciences, CBSH G.B. Pant University of Agriculture & Technology, Pantnagar, Uttarakhand, India

Contributors Mushineni Ashajyothi ICAR-Central Agroforestry Research Institute, Jhansi, Uttar Pradesh, India D. J. Bagyaraj Centre for Natural Biological Resources and Community Development (CNBRCD), Bangalore, Karnataka, India Saroj Belbase Department of Mycology & Plant Pathology, Institute of Agricultural Sciences, Banaras Hindu University, Varanasi, Uttar Pradesh, India Alka Bharati ICAR-Central Agroforestry Research Institute, Jhansi, Uttar Pradesh, India Akhilendra Pratap Bharti Plant-Microbe Interaction and Rhizosphere Biology Lab, ICAR-National Bureau of Agriculturally Important Microorganisms, Maunath Bhanjan, Uttar Pradesh, India R. K. Bhavyasree ICAR-Regional Research Station, Gurdaspur, Punjab Agriculture University, Gurdaspur, Punjab, India Dawa Dolma Bhutia Department of Mycology and Plant Pathology, Institute of Agricultural Sciences, Banaras Hindu University, Varanasi, Uttar Pradesh, India

Editors and Contributors

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Jharjhari Chakma Department of Mycology and Plant Pathology, Institute of Agricultural Sciences, Banaras Hindu University, Varanasi, Uttar Pradesh, India Sharani Choudhury ICAR-National Institute for Plant Biotechnology, Indian Agricultural Research Institute, New Delhi, India Gowardhan Kumar Chouhan Institute of Environment and Sustainable Development, Banaras Hindu University, Varanasi, Uttar Pradesh, India Theodore C. Crusberg Department of Biology and Biotechnology, Worcester Polytechnic Institute, Worcester, MA, USA Brookline, MA, USA Suresh Deka Environmental Biotechnology Laboratory, Resource Management and Environment Section, Life Sciences Division, Institute of Advanced Study in Science and Technology (IASST), Guwahati, Assam, India Sarita Devi Division of Biotechnology, CSIR-Institute of Himalayan Bioresource Technology, Palampur, Himachal Pradesh, India Manoj K. Dhar School of Biotechnology, University of Jammu, Jammu, Jammu and Kashmir, India Prerna Dobhal Department of Plant Pathology, College of Agriculture, G. B. Pant University of Agriculture and Technology, Pantnagar, Uttarakhand, India Anamika Dubey Metagenomics and Secretomics Research Laboratory, Department of Botany, Dr. HarisinghGour University (A Central University), Sagar, Madhya Pradesh, India Anand Kumar Gaurav Institute of Environment and Sustainable Development, Banaras Hindu University, Varanasi, Uttar Pradesh, India Madhurankhi Goswami Environmental Biotechnology Laboratory, Resource Management and Environment Section, Life Sciences Division, Institute of Advanced Study in Science and Technology (IASST), Guwahati, Assam, India Life Sciences Division, Department of Molecular Biology and Biotechnology, Cotton University, Guwahati, Assam, India Soma Gupta ICAR-Indian Institute of Seed Science, Maunath Bhanjan, Uttar Pradesh, India Gary E. Harman Cornell University, Geneva, NY, USA Deepanshu Jayaswal ICAR-Indian Institute of Seed Science, Maunath Bhanjan, Uttar Pradesh, India Subhesh Saurabh Jha Centre of Advanced Study in Botany, Institute of Science, Banaras Hindu University, Varanasi, Uttar Pradesh, India

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Editors and Contributors

Prem Lal Kashyap ICAR-Indian Institute of Wheat & Barley Research (IIWBR), Karnal, Haryana, India Sanjana Kaul School of Biotechnology, University of Jammu, Jammu, Jammu and Kashmir, India Gopi Kishan ICAR-Indian Institute of Seed Science, Maunath Bhanjan, Uttar Pradesh, India Ashutosh Kumar ICAR-Indian Institute of Seed Science, Maunath Bhanjan, Uttar Pradesh, India Ashwani Kumar Metagenomics and Secretomics Research Laboratory, Department of Botany, Dr. Harisingh Gour University (A Central University), Sagar, Madhya Pradesh, India Gagan Kumar Krishi Vigyan Kendra, Rajendra Prasad Central Agriculture University, Pusa, Samastipur, Bihar, India Poonam Kumari Division of Agrotechnology, CSIR-Institute of Himalayan Bioresource Technology, Palampur, Himachal Pradesh, India Sudeepa Kumari Institute of Environment and Sustainable Development, Banaras Hindu University, Varanasi, Uttar Pradesh, India Sunita Kumari ICAR-Indian Institute of Seed Science, Maunath Bhanjan, Uttar Pradesh, India Kanchan Kumar Centre of Advanced Study in Botany, Banaras Hindu University, Varanasi, Uttar Pradesh, India Ravindra Kumar ICAR-Indian Institute of Wheat and Barley Research, Karnal, Haryana, India Sachin Kumar Department of Plant Pathology, Sardar Vallabhbhai Patel University of Agriculture & Technology, Meerut, Uttar Pradesh, India Sandeep Kumar Division of Crop Protection, Indian Institute of Pulses Research, Kalyanpur, Kanpur, Uttar Pradesh, India Sanjay Kumar ICAR-Indian Institute of Seed Science, Maunath Bhanjan, Uttar Pradesh, India Vivek Kumar Himalayan School of Biosciences, Swami Rama Himalayan University, Jolly Grant, Dehradun, Uttarakhand, India Prity Kushwaha ICAR-National Bureau of Agriculturally Microorganisms (NBAIM), Maunath Bhanjan, Uttar Pradesh, India

Important

Ayush Lepcha Institute of Environment and Sustainable Development, Banaras Hindu University, Varanasi, Uttar Pradesh, India

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José López-Bucio Instituto de Investigaciones Químico-Biológicas, Universidad Michoacana de San Nicolás de Hidalgo, Morelia, Michoacán, Mexico Deepti Malviya Plant-Microbe Interaction and Rhizosphere Biology Lab, ICARNational Bureau of Agriculturally Important Microorganisms, Kushmaur, Maunath Bhanjan, Uttar Pradesh, India Asit Mandal ICAR-Indian Institute of Soil Science, Bhopal, Madhya Pradesh, India Raghavendra Reddy Manda Wageningen University & Research, Wageningen, the Netherlands C. M. Mehta School of Agriculture, Lovely Professional University, Phagwara, Punjab, India Manisha Mishra Department of Botany, DDU Gorakhpur University, Gorakhpur, Uttar Pradesh, India Monika Mishra Division of Crop Protection, Indian Institute of Pulses Research, Kalyanpur, Kanpur, Uttar Pradesh, India R. K. Mishra Division of Crop Protection, Indian Institute of Pulses Research, Kalyanpur, Kanpur, Uttar Pradesh, India Arpan Mukherjee Institute of Environment and Sustainable Development, Banaras Hindu University, Varanasi, Uttar Pradesh, India T. Muthukumar Root and Soil Biology Laboratory, Department of Botany, Bharathiar University, Coimbatore, Tamil Nadu, India Gaurav Pal Centre of Advanced Study in Botany, Banaras Hindu University, Varanasi, Uttar Pradesh, India Govind Pal ICAR-Indian Institute of Seed Science, Maunath Bhanjan, Uttar Pradesh, India Namrata Pal ICMR-National Institute for Research in Environmental Health, Bhauri, Bhopal, Madhya Pradesh, India Sonika Pandey Division of Crop Protection, Indian Institute of Pulses Research, Kalyanpur, Kanpur, Uttar Pradesh, India K. Pandiyan Ginning Training Centre, ICAR-Central Institute for Research on Cotton Technology (CIRCOT), Nagpur, Maharashtra, India Jai Singh Patel Department of Botany, Institute of Science, Banaras Hindu University, Jamuhar, Bihar, India Ved Prakash Department of Biotechnology, Motilal Nehru National Institute of Technology Allahabad, Prayagraj, India

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Editors and Contributors

Durga Prasad Department of Plant Pathology, Sardar Vallabhbhai Patel University of Agriculture & Technology, Meerut, Uttar Pradesh, India Parichita Priyadarshini ICAR-Crop Improvement Division, Indian Grassland and Fodder Research Institute, Jhansi, Uttar Pradesh, India Krishna Kumar Rai Molecular Biology Section, Centre of Advanced Study in Botany, Institute of Science, Banaras Hindu University, Varanasi, Uttar Pradesh, India L. C. Rai Molecular Biology Section, Centre of Advanced Study in Botany, Institute of Science, Banaras Hindu University, Varanasi, Uttar Pradesh, India Ruchi Rai Molecular Biology Section, Centre of Advanced Study in Botany, Institute of Science, Banaras Hindu University, Varanasi, Uttar Pradesh, India V. Rajeshkannan Rhizosphere Biology Laboratory, Department of Microbiology, Bharathidasan University, Tiruchirappalli, Tamil Nadu, India Vinita Ramtekey ICAR-Indian Institute of Seed Science, Maunath Bhanjan, Uttar Pradesh, India Meenakshi Rana School of Agriculture, Lovely Professional University, Phagwara, Punjab, India Shweta Rana Department of Physical and Natural Sciences, FLAME University, Pune, India Md Mahtab Rashid Department of Plant Pathology, Bihar Agricultural University, Sabour, Bhagalpur, Bihar, India Utkarsh Singh Rathore Division of Crop Protection, Indian Institute of Pulses Research, Kalyanpur, Kanpur, Uttar Pradesh, India Gustavo Ravelo-Ortega Instituto de Investigaciones Químico-Biológicas, Universidad Michoacana de San Nicolás de Hidalgo, Morelia, Michoacán, Mexico Paramanand Sahni ICAR-Indian Institute of Seed Science, Maunath Bhanjan, Uttar Pradesh, India Asha Sahu ICAR-Indian Institute of Soil Science, Bhopal, Madhya Pradesh, India Nisha Sahu ICAR-Indian Institute of Soil Science, Bhopal, Madhya Pradesh, India Pramod K. Sahu Plant-Microbe Interaction and Rhizosphere Biology Lab, ICARNational Bureau of Agriculturally Important Microorganisms, Kushmaur, Maunath Bhanjan, Uttar Pradesh, India Ankita Sarkar Department of Mycology & Plant Pathology, Institute of Agricultural Sciences, Banaras Hindu University, Varanasi, Uttar Pradesh, India

Editors and Contributors

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Anil K. Saxena Plant-Microbe Interaction and Rhizosphere Biology Lab, ICARNational Bureau of Agriculturally Important Microorganisms, Kushmaur, Maunath Bhanjan, Uttar Pradesh, India Nitish Sharma Shi Ram Swaroop Memorial University, Lucknow, Uttar Pradesh, India Poonam Sharma ICAR-Indian Institute of Soil Science, Bhopal, Madhya Pradesh, India ICMR-National Institute for Research in Environmental Health, Bhauri, Bhopal, Madhya Pradesh, India Samarth Sharma Department of Biotechnology, Motilal Nehru National Institute of Technology Allahabad, Prayagraj, Uttar Pradesh, India Shivesh Sharma Department of Biotechnology, Motilal Nehru National Institute of Technology Allahabad, Prayagraj, Uttar Pradesh, India Tanwi Sharma School of Biotechnology, University of Jammu, Jammu, Jammu and Kashmir, India Arvind Nath Singh ICAR-Indian Institute of Seed Science, Maunath Bhanjan, Uttar Pradesh, India Harsh V. Singh Plant-Microbe Interaction and Rhizosphere Biology Lab, ICARNational Bureau of Agriculturally Important Microorganisms, Kushmaur, Maunath Bhanjan, Uttar Pradesh, India Prem Pratap Singh Centre of Advanced Study in Botany, Institute of Science, Banaras Hindu University, Varanasi, Uttar Pradesh, India Ramji Singh Department of Plant Pathology, Sardar Vallabhbhai Patel University of Agriculture & Technology, Meerut, Uttar Pradesh, India Sandeep Kumar Singh Centre of Advanced Study in Botany, Institute of Science, Banaras Hindu University, Varanasi, Uttar Pradesh, India Satyendra Pratap Singh Department of Mycology and Plant Pathology, Institute of Agricultural Sciences, Banaras Hindu University, Varanasi, Uttar Pradesh, India Saurabh Singh Institute of Environment and Sustainable Development, Banaras Hindu University, Varanasi, Uttar Pradesh, India Shailendra Singh Plant-Microbe Interaction and Rhizosphere Biology Lab, ICARNational Bureau of Agriculturally Important Microorganisms, Kushmaur, Maunath Bhanjan, Uttar Pradesh, India Shilpi Singh Molecular Biology Section, Centre of Advanced Study in Botany, Institute of Science, Banaras Hindu University, Varanasi, Uttar Pradesh, India

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Editors and Contributors

Udai B. Singh Plant-Microbe Interaction and Rhizosphere Biology Lab, ICARNational Bureau of Agriculturally Important Microorganisms, Kushmaur, Maunath Bhanjan, Uttar Pradesh, India ICAR-National Bureau of Agriculturally Important Microorganisms, Maunath Bhanjan, Uttar Pradesh, India Vinit Pratap Singh College of Agriculture, Azamgarh Campus, Acharya Narendra Dev University of Agriculture & Technology, Faizabad, Uttar Pradesh, India N. Sreeshma ICAR-National Institute for Plant Biotechnology, Indian Agricultural Research Institute, New Delhi, India Deepa Srivastava Department of Botany, DDU Gorakhpur University, Gorakhpur, Uttar Pradesh, India Ruchi Srivastava ICAR-National Bureau of Agriculturally Microorganisms (NBAIM), Maunath Bhanjan, Uttar Pradesh, India

Important

Seweta Srivastava School of Agriculture, Lovely Professional University, Phagwara, Punjab, India C. S. Sumathi Department of Chemistry and Biosciences, Srinivasa Ramanujan Centre, SASTRA Deemed to be University, Kumbakonam, Tamil Nadu, India Basavaraj Teli Department of Mycology & Plant Pathology, Institute of Agricultural Sciences, Banaras Hindu University, Varanasi, Uttar Pradesh, India Jyotsana Tilgam ICAR-National Bureau of Agriculturally Important Microorganisms, Kushmaur, Maunath Bhanjan, Uttar Pradesh, India ICAR-National Institute for Plant Biotechnology, Indian Agricultural Research Institute, Kushmaur, Maunath Bhanjan, Uttar Pradesh, India ICAR-National Institute for Plant Biotechnology, Indian Agricultural Research Institute, New Delhi, India Anita Tilwari Madhya Pradesh Council of Science and Technology, Bhopal, Madhya Pradesh, India Ajay Tomar Department of Plant Pathology, Sardar Vallabhbhai Patel University of Agriculture & Technology, Meerut, Uttar Pradesh, India Durgesh Kumar Tripathi Amity Institute of Organic Agriculture, Amity University, Noida, Uttar Pradesh, India Kulbhushan Mani Tripathi Division of Crop Protection, Indian Institute of Pulses Research, Kalyanpur, Kanpur, Uttar Pradesh, India Sneha Tripathi Department of Biotechnology, Motilal Nehru National Institute of Technology Allahabad, Prayagraj, Uttar Pradesh, India Anand Verma Centre of Advanced Study in Botany, Banaras Hindu University, Varanasi, Uttar Pradesh, India

Editors and Contributors

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Jay Prakash Verma Institute of Environment and Sustainable Development, Banaras Hindu University, Varanasi, Uttar Pradesh, India Satish Kumar Verma Centre of Advanced Study in Botany, Banaras Hindu University, Varanasi, Uttar Pradesh, India H. S. Viswanath Department of Plant Pathology, Sardar Vallabhbhai Patel University of Agriculture & Technology, Meerut, Uttar Pradesh, India Dhuni Lal Yadav Plant Pathology, Agricultural Research Station, Agriculture University, Kota, Rajasthan, India Sudheer Kumar Yadav Narayan Institute of Agricultural Sciences, Gopal Narayan Singh University, Jamuhar, Bihar, India

1

Evolution of the Knowledge and Practice of Endophytic Microorganisms for Enhanced Agricultural Benefit and Environmental Sustainability Gary E. Harman

Abstract

Microorganisms have been known for more than a century to provide multiple benefits to plants. A key to understanding the benefits imparted is knowledge of the specific kinds of interactions that occur continuously between plants and microorganisms. This chapter reviews how knowledge of these has evolved over time, what the resulting benefits are, and how microorganisms can be used to benefit plant agriculture and the natural environment.

1.1

Introduction

Fundamental to any discussion of benefits is the concept of holobionts. Plants like any other “higher” organism do not exist as independent entities; rather they are the visible part of an association of the plant and the microorganisms that colonize it, becoming part of an ecological whole (Margulis and Fester 1991). Most of these associations are beneficial, especially those that colonize the interior spaces of plants. Such organisms are termed endophytes, meaning that they live within plants. Plant–microbial entities where the microbes are endophytic and highly beneficial, when selected microorganisms have been purposefully introduced to enrich and enhance the plant’s microbiome, we have described as Enhanced Plant Holobionts (EPHs) (Harman and Uphoff 2019). There have been a number of advances in knowledge and understanding regarding such associations that justify a different paradigm for conceiving and practicing modern agriculture, one that does not treat plants as isolated entities, to be improved

G. E. Harman (*) Cornell University, Geneva, NY, USA e-mail: [email protected] # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2022 U. B. Singh et al. (eds.), Re-visiting the Rhizosphere Eco-system for Agricultural Sustainability, Rhizosphere Biology, https://doi.org/10.1007/978-981-19-4101-6_1

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Fig. 1.1 Types of interactions between plants, microbial agents, and other microorganisms. Except for Rhizobia and mycorrhizal fungi, early views of the interactions centered on the interactions between agents and other microorganisms. As understanding evolved, the plant–agent interaction was appreciated more. We now know that many benefits to plants, including disease and pest control, alleviation of abiotic stresses, nutritional benefits, and increased photosynthesis, occur as a consequence of systemic responses of plants due to the plant–agent interaction

genetically and provided with external inputs to improve plant growth and protection. Important steps in the development of this alternative understanding of how to advance agriculture are provided in bullet form below. • An understanding that microorganisms can be highly beneficial to plants. • A more sophisticated view of the interactions among pathogens or pests, the plant, and beneficial microbial agents. These relationships are shown diagrammatically in Fig. 1.1. • Appreciation that some microorganisms are endophytic, residing not just around or on plants, but actually within plant organs, tissues, and cells. • Seeing that many microorganisms are multifunctional vis-à-vis plants and impart many diverse advantages to their hosts. • Recognizing that there can be many advantages from this association for plant agriculture and beyond this for the natural environment, including abatement of climate change. This review is divided into sections that describe the history and evolution of these interactions, considering also how they affect social and agricultural sustainability.

1.2

History and Concepts of Microbial–Plant Interactions

Some organisms have been known for more than a century to be endophytic. Mycorrhizal fungi, which live symbiotically rather than parasitically within plant roots, were first named and described in 1882 (Kamieński 1882). Rhizobium, a genus

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of bacteria that benefit leguminous and other plants, was first described in 1889 (Young et al. 2001). The endophytic nature of many other organisms that favor plant growth and health has been reported later. For example, Trichoderma were first described as rhizosphere-competent in 1988 (Ahmad and Baker 1988) after some, but by no means all, were shown to be endophytic (Chao et al. 1986). Difference in the abilities of some strains but not others of the same species is an important concept that will be emphasized throughout this review. Many other organisms contain strains that are endophytic, including both fungi and bacteria. Specific genera are Piriformospora indica (Gill et al. 2016), Pseudomonas (Pieterse et al. 2014), and Gliocladium rosea (Sutton and Peng 1993). Many of these organisms colonize only the roots of plants and are restricted to them; but G. rosea, for example, also colonizes above-ground plant parts. Some Trichoderma strains also colonize above-ground parts of plants. For example, some of these strains colonize the stems and leaves of cacao, while these same strains colonize only roots of pepper plants (Bae et al. 2011).

1.3

Benefits to Plants

Several aspects of the benefits that microorganisms provide to plants are not a consequence of the endophytic nature of the microorganisms involved, but are a consequence of other mechanisms. These include mycoparasitism, by which certain microorganisms protect plants by infesting pathogens, which is well described in Chet (1987). Various types of competition between beneficial microorganisms and plant pathogens occur, whereby the latter are curbed by competition for space and/or for nutrients. This can be difficult to prove, but it undoubtedly occurs. Competition for iron nutrients in the soil is a special case, well documented, as described in Hubbard et al. (1983) and Trapet et al. (2016). Since these are well described elsewhere, they will not be covered in this chapter. Various mechanisms whereby microorganisms benefit plants have been reviewed in Harman and Uphoff (2019) and are mentioned only in passing here.

1.3.1

Control of Plant Diseases and Pests, and Alleviation of Abiotic Stress

Control of pests and diseases and of abiotic stresses is considered together since similar systems and mechanisms are activated for both kinds of stresses. Both happen via microbes inducing modifications in plant gene expression and impacts on the proteins encoded from the plant’s genome. Endophytic microorganisms can induce systemic responses throughout the plant that are evoked by elicitor molecules; such responses are elicited by many endophytes. These elicitors have been summarized and reviewed, for example, in Chi et al. (2005), Waller et al. (2005), Lorito et al. (2010), Pieterse et al. (2014), Mo et al. (2016), Fukami et al. (2018), and Harman and Uphoff (2019). These references cover Rhizobium,

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Azospirillum, Piriformospora indica, Trichoderma, Pseudomonas, and mycorrhizal fungi, demonstrating the widespread occurrence of similar systems. The references include induced plant resistance to both biotic and abiotic stresses. An important aspect of all of these mechanisms is control of reactive oxygen species (ROS). ROS are strongly active molecules that damage almost all of the plant’s physiological systems, including photosynthetic elements, proteins, and nucleic acids. The plant’s production of ROS is induced by both biotic and abiotic stresses, and even by the process of photosynthesis if high light levels result in overexcitement of electron flows beyond the capacity of the plant’s photosystems to absorb them (Nath et al. 2016). Plants minimize the damaging effects of ROS by producing reducing compounds and enzymes that detoxify ROS, converting it to less damaging molecules (Mittler 2002). All of the endophytes mentioned above have this capability in common, also helping to control ROS (Waller et al. 2005; Mastouri et al. 2010; Pieterse et al. 2014; Mo et al. 2016).

1.3.2

Improvements in Photosynthesis

Photosynthesis converts sunlight into energy by fixing carbon. Both energy and carbon are essential to all life on Earth. Increased photosynthesis is essential if we are to meet increasing demand for food and fiber by doubling plant productivity (Ort et al. 2015). This need is particularly acute because increases in crop productivity have stalled at the global level (Foyer et al. 2017). Efforts to increase the photosynthetic capacity of plants by making genetic modifications have resulted in more frustration than success (Foyer et al. 2017). Engaging endophytic microorganisms in enhancing photosynthesis is the only evident method currently available to increase essential process. Many or perhaps most bacterial or fungal endophytes have the capacity to improve photosynthesis. Pertinent references include Mo et al. (2016) for mycorrhizal fungi and Chi et al. (2005) for Rhizobium in cereals. A complete description of events occurring with Trichoderma is provided in Harman et al. (2019). Like resistance to biotic and abiotic stresses, these fungi induce systemic responses that result in maintenance of and an increase in photosynthetic elements, including photoactive pigments such as chlorophyll and carotenoids and the proteins involved in synthesis of most of the necessary machinery for photosynthesis. An important factor in this improvement is an increased level of gene expression and of the proteins they encode. The gene transcripts involved are identified in Doni et al. (2019) and Harman et al. (2019). Another aspect of the increased photosynthetic capacity of plants is the maintenance of their existing capabilities. The previous section described the harmful effects of ROS on most physiological systems in plants. Curbing these effects is an important part of the contribution that endophytes make to enhance photosynthetic capacity of plants that they have colonized.

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Evolution of the Knowledge and Practice of Endophytic Microorganisms. . .

1.3.3

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Enhanced Nutrition

Plant growth is frequently enhanced by the activities of endophytic microorganisms. One reason for this enhancement results from improvements in nutrient uptake and acquisition. The Rhizobiaceae–legume interaction results in fixation of atmospheric nitrogen in nodules on roots and alleviates much of the need for added nitrogen from fertilizers. This has tremendous environmental and economic impacts, since the production of nitrogen fertilizers is expensive, requires substantial amounts of fossil fuels to produce, and runoff of excess nitrates into waterways results in the growth of undesirable algae that can result in fish kills and other environmental impacts (Anonymous 2020). Some endophytic microorganisms can increase plant-available N levels on a per-area basis because they contribute to increased total biomass (Harman and Uphoff 2019). Some endophytes solubilize nutrients in soil and transfer these to plants, thereby improving the nutrient status of plants. Mycorrhizae are well known for their ability to raise the phosphorus status of plants as well as that of other nutrients (Parniske 2008). Other endophytic organisms, such as Trichoderma, also solubilize important plant nutrients, making them available to plants (Altomare et al. 1999).

1.3.4

Enhanced Plant Growth and Yield

As a consequence of all of these mechanisms by which endophytes improve plant growth, plants that have enhanced, larger, more diverse, and more active microbiomes frequently are larger and yield more. The literature contains numerous references to this, reviewed in Harman and Uphoff (2019). Greater yields provide more food to a growing world population and are therefore essential for both agricultural and societal sustainability.

1.4

Improvements in Soil Health and Sustainability

Endophytic microorganisms provide marked improvements to soil health, which contributes to agricultural sustainability. Enhanced photosynthesis is required for this and for the other benefits described in this review. All of these require energy and fixed carbon compounds, and these must come from photosynthesis (Shoresh and Harman 2008). Soil health benefits include higher levels of organic compounds in the soil that enhance microbial diversity (Li et al. 2020). In various studies, a combination of factors including minimal tillage and cover cropping has resulted in an increase in soil organic matter (SOM). Greater SOM improves yields and offers a potential for reducing greenhouse gases, especially CO2 (Paustian et al. 2016). However, a systems approach is required, not just introducing a single change. If the farming system is not modified, carbon put into the soil may be released as quickly as it is delivered due to enhanced microbial respiration at least

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in the absence of cover cropping (Anonymous 2014). So, depending on the farming systems used, carbon sequestration may or may not occur. None the less, increased fixed carbon added to the soil usually results in improved soil health. The combination of cover crops plus reduced tillage can result in improvements in water infiltration, erosion control, and increased formation of soil aggregates (Schmidt et al. 2018, 2019). Soil aggregates are particularly important because these aggregates protect organic matter from soil microbes, thereby minimizing respiratory loss of fixed carbon (Six et al. 1998; Olchin et al. 2008). Thus, while carbon sequestration can occur, a systems approach needs to be followed to insure that the storage of carbon in the soil results (King 2011).

1.5

Conclusion

This review demonstrates the evolution of knowledge and practice to enhance agricultural benefits and environmental sustainability. Rhizobia and mycorrhizae have been known for about a century to colonize interior spaces of roots. However, studies on other microorganisms have considered primarily the interactions between different microbes and focused primarily on the control of diseases. Beginning in the 1990s, an appreciation was generated for the interactions between plants and microorganisms and within the diverse communities of microorganisms around, on, and within plants. Over this same period, some microorganisms, including fungi and bacteria, were demonstrated to be endophytic and to function as true symbionts. A very important component of this understanding was the knowledge that these organisms cause systemic reactions in plants and that these effects provide large benefits to plants and to plant agriculture. These interactions result in increased resistance to biotic and abiotic stresses, improve the nutrient status of plants, and increase their photosynthetic capabilities. These are becoming increasingly important for improving food production for a growing world and for creating environmental sustainability.

References Ahmad JS, Baker R (1988) Rhizosphere competence of benomyl-tolerant mutants of Trichoderma spp. Can J Microbiol 34:694–696 Altomare C, Norvell WA, Björkman T, Harman GE (1999) Solubilization of phosphates and micronutrients by the plant-growth-promoting and biocontrol fungus Trichoderma harzianum Rifai 1295-22. Appl Environ Microbiol 65:2926–2933 Anonymous. (2014). No-till soil organic carbon sequestration rates published. (Report on research at the University of Illinois College of Agricultural, Consumer and Environmental Sciences.) Science Daily. https://www.sciencedaily.com/releases/2014/04/140418161344.htm Anonymous. (2020). Gulf of Mexico dead zone Bae H, Roberts DP, Lim H-S, Strem MD, Park S-C, Ryu C-M, Melnick R, Bailey BA (2011) Endophytic Trichoderma isolates from tropical environments delay disease onset and induce

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resistance against Phytophthora capsici in hot pepper using multiple mechanisms. Mol PlantMicrobe Interact 24:336–351 Chao WL, Nelson EB, Harman GE, Hoch HC (1986) Colonization of the rhizosphere by biological control agents applied to seeds. Phytopathology 76:60–65 Chet I (ed) (1987) Innovative approaches to plant disease control. John Wiley, New York Chi F, Shen S-H, Cheng H-P, Jing Y-X, Yanni YG, Dazzo FB (2005) Ascending migration of endophytic rhizobia, from roots to leaves, inside rice plants and assessment of benefits to rice growth physiology. Appl Environ Microbiol 71:7271–7278 Doni F, Fathurrahman F, Mispan MS, Suhaimi M, Yussof WMW, Uphoff N (2019) Transciptome profiling of rice seedlings inoculated with symbiotic fungus Trichoderma asperellum SL2. J Plant Growth Reg 38:1507–1515. https://doi.org/10.1007/s00344-019-09952-7 Foyer CH, Ruban AV, Nixon PJ (2017) Photosynthesis solutions to enhance productivity. Philos Trans R Soc London B Biol Sci 372:20160374 Fukami J, de la Osa C, Javier OF, Megias M, Hungria M (2018) Co-inoculation of maize with Azospirillum brasilense and Rhizobium tropici as a strategy to mitigate salinity stress. Funct Plant Biol 45(3):328–339 Gill SS, Gill R, Trivedi DK, Anjum NA, Sharma KK, Ansari MW, Ansari AA, Johri AK, Prasad R, Pereira E, Varma A, Tuteja N (2016) Piriformospora indica: potential and significance in plant stress tolerance. Front Microbiol 7:332 Harman GE, Uphoff N (2019) Advantages and methods of using symbiotic microbes to enhance plant agriculture and the environment. Scientifica 2019:9106395. https://doi.org/10.1155/2019/ 9106395 Harman GE, Doni F, Khadka RB, Uphoff N (2019) Endophytic strains of Trichoderma increase plants' photosynthetic capability. J Appl Microbiol. https://doi.org/10.1111/jam.14368 Hubbard JP, Harman GE, Hadar Y (1983) Effect of soilborne Pseudomonas sp. on the biological control agent, Trichoderma hamatum, on pea seeds. Phytopathology 73:655–659 Kamieński F (1882) Les organes végétatifs de Monotropa hypopitys L.. Mémoires de la Société nat. des Sciences naturelles et mathém. de Cherbourgser. 3, tom. 24. (Republished and translated, in: Berch SM, Massicotte HB, Tackaberry LE. 2005. Re-publication of a translation of ‘The vegetative organs of Monotropa hypopitys L.’ published by F. Kamienski in 1882, with an update on Monotropa mycorrhizas. Mycorrhiza 15:323–332 King GM (2011) Enhancing soil carbon storage for carbon remediation: potential contributions and constraints by microbes. Trends Microbiol 19:75–84 Li Y, Li Z, Chang SX, Cui S, Jagadamma S, Zhang Q, Cai Y (2020) Residue retention promotes soil carbon accumulation in minimum tillage systems: implications for conservation agriculture. Sci Total Environ 740:140147 Lorito M, Woo SL, Harman GE, Monte E (2010) Translational research on Trichoderma: from 'omics to the field. Annu Rev Phytopathol 48:395–417 Margulis L, Fester R (1991) Symbiosis as a source of evolutionary innovation. MIT Press, Cambridge, MA Mastouri F, Bjorkman T, Harman GE (2010) Seed treatments with Trichoderma harzianum alleviate biotic, abiotic and physiological stresses in germinating seeds and seedlings. Phytopathology 100:1213–1221 Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410 Mo Y, Wang Y, Yang R, Zheng J, Liu C, Li H, Ma J, Zhang Y, Wei C, Zhang X (2016) Regulation of plant growth, photosynthesis, antioxidation and osmosis by an arbuscular mycorrhizal fungus in watermelon seedlings under well-watered and drought conditions. Front Plant Sci 7:644 Nath M, Bhatt DD, Prasad R, Gill SS, Anjum NA, Tuteja N (2016) Reactive oxygen species: Generation-scavenging and signaling during plant-arbuscular mycorrhizal and Piriformospora indica interaction under stress condition. Front Plant Sci 7:1574 Olchin GP, Ogle S, Frey SD, Filley TR, Paustian K, Six J (2008) Residue carbon stabilization in soil aggregates of no-till and tillage management of dryland cropping systems. Soil Sci Soc Am J 72: 507–513

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Ort DR, Merchant SS, Alric J, Barkan A, Blankenship RE, Bock R, Croce R, Hanson MR, Hibberd JM, Long SP, Moore TA, Moroney J, Niyogi KK, Parry MAJ, Peralta-Yahya PP, Prince RC, Redding KE, Spalding MH, van Wijk KJ, Vermaas WFJ, von Caemmerer S, Weber APM, Yeates TO, Yuan JS, Zhu XG (2015) Redesigning photosynthesis to sustainably meet global food and bioenergy demand. PNAS(USA) 112:8529–8536 Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775 Paustian K, Campell N, Dorich C, Marx E, Swan A (2016) Assessment of potential greenhouse gas mitigation from changes to crop root management and architecture. Booz Allen Hamilton, Washington DC Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, Van Wees SCM, Bakker PAHM (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347–375 Schmidt R, Gravuer K, Bossange AV, Mitchell J, Scow K (2018) Long-term use of cover crops and no-till shift soil microbial community life strategies in agricultural soil. PLoS One 13:e0192953 Schmidt R, Mitchell J, Scow K (2019) Cover cropping and no-till increase diversity and symbiotroph:saprotroph ratios of soil fungal communities. Soil Biol Biochem 129:99–109 Shoresh M, Harman GE (2008) The relationship between increased growth and resistance induced in plants by root colonizing microbes. Plant Signal Behav 3:737–739 Six J, Elliott ET, Paustian K, Doran JW (1998) Aggregation and soil organic matter accumulation in cultivated and native grassland soils. Soil Sci Soc Am J 62:1367–1377 Sutton JC, Peng G (1993) Biocontrol of Botrytis cinerea in strawberry leaves. Phytopathology 83: 615–621 Trapet P, Avoscan L, Klinguer A, Pateyron S, Citerne S, Chervin C, Mazurier S, Lemanceau P, Wendehenne D, Besson-Bard A (2016) The Pseudomas fluorescens siderophore Pyoverdine weakens Arabidopsis thaliana defense in favor of growth in iron-deficient conditions. Plant Physiol (Rockville) 171:675–693 Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Hueckelhoven R, Neumann C, von Wettstein D, Franken P, Kogel K-H (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. PNAS USA 102:13386–13391 Young JM, Kuykendall LD, Martinez-Romero E, Kerr A, Sawada H (2001) A revision of Rhizobium Frank 1889, with an emended description of the genus, and the inclusion of all species of Agrobacterium Conn 1942 and llorhizobium undicola de Lajudie et al. 1998 as new combinations: Rhizobium radiobacter, R. rhizogenes, R. rubi, R. undicola and R. vitis. Int J Syst Evol Microbiol 51:89–103

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Mycorrhizosphere Revisited: Multitrophic Interactions T. Muthukumar, C. S. Sumathi, V. Rajeshkannan, and D. J. Bagyaraj

Abstract

The soil and plant roots provide natural habitats for a diverse assemblage of microorganisms that play an important role in nutrient cycling and other ecosystem processes. The services provided by these microbial processes are important for maintaining the diversity and functioning of ecosystems worldwide. In this chapter, we examine the information available on the plant–mycorrhizal fungal interactions in soil with a focus on the mycorrhizosphere. Available evidences do indicate that the microbial populations in the mycorrhizosphere could substantially differ from those of the rhizosphere and surrounding bulk soil. Further, the various microbial interactions in the mycorrhizosphere are important for the development and health of plants both in the natural and anthropogenic ecosystems. The microorganisms solubilize or decompose the complex macromolecules in the mycorrhizosphere and make the nutrients available for plants and other microorganisms. Some of the bacteria residing in the mycorrhizosphere could also act as mycorrhiza helper bacteria and plant

T. Muthukumar Root and Soil Biology Laboratory, Department of Botany, Bharathiar University, Coimbatore, Tamil Nadu, India C. S. Sumathi Department of Chemistry and Biosciences, Srinivasa Ramanujan Centre, SASTRA Deemed to be University, Kumbakonam, Tamil Nadu, India V. Rajeshkannan Rhizosphere Biology Laboratory, Department of Microbiology, Bharathidasan University, Tiruchirappalli, Tamil Nadu, India D. J. Bagyaraj (*) Centre for Natural Biological Resources and Community Development (CNBRCD), Bangalore, Karnataka, India # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2022 U. B. Singh et al. (eds.), Re-visiting the Rhizosphere Eco-system for Agricultural Sustainability, Rhizosphere Biology, https://doi.org/10.1007/978-981-19-4101-6_2

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growth-promoting rhizobacteria with numerous functions. The carbon exuded by the plants directly into the rhizosphere and the fungi in the hyphosphere play a pivotal role in maintaining the diversity and activities of microorganisms in the mycorrhizosphere. At present we are only looking at a glimpse of the complex intricate interactions that are occurring in the mycorrhizosphere. However, evidences available so far suggest that multitrophic interactions in the mycorrhizosphere play a significant role in maintaining the health and productivity of plants and soils in sustainable natural and agroecosystems.

2.1

Introduction

The plant root is necessary for maintaining soil integrity and fertility besides anchoring and obtaining soil resources. The development of roots unleashes a number of physicochemical and biological activities in the soil. These changes are brought about either by the removal or addition of substances to the soil by plant roots. One of the most striking changes that happen in soil biology in response to root development is the alterations in the population and activities of microorganisms. Plant roots are frequently associated with archaea, bacteria, and fungi along with a myriad of other organisms. The microorganisms influenced by plant roots play a key role in making available the various nutrients required for the normal growth and development of plants and also are important for maintaining the fertility of the soil. Plants thus rely on microorganisms in spite of having several physiological and anatomical adaptations of their own. Among the microbes interacting with plant roots, some colonize the roots and substantially modify the morphology and nature of the root system. The microorganisms colonizing root tissues are placed better to influence various plant processes than those that are present over or surrounding the roots (Hassani et al. 2018). Therefore, plant roots are not individual entities but are composite organs that act as niches for diverse microbes. This ability of plants to establish symbiosis with different types of organisms enabled them to colonize and thrive in stressful terrestrial habitats (Morris et al. 2018). Among the different types of microorganisms establishing symbiosis with plant roots, the most common and widespread are the mycorrhizal fungi. The fungi belonging to diverse fungal groups like the Ascomycota, Basidiomycota, and Mucoromycota can associate with more than 90% of plant species (Spatafora et al. 2016; Brundrett and Tedersoo 2018). The symbiosis established between mycorrhizal fungi and plant roots greatly varies in their structure and there are seven types of mycorrhiza recognized namely the ecto, arbuscular, orchid, arbutoid, monotropoid, ericoid, and ectendomycorrhiza. Although some types of mycorrhizal association are restricted to certain plant families (ericoid, arbutoid, monotropoid, orchid) or to specific plant growth forms (ecto, ectendo), arbuscular mycorrhiza is more common as it occurs in more than 72% of the extant plant taxa and establishes an association with diverse plant families and growth habits (Brundrett and Tedersoo 2018).

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Though the fungus is obligately dependent on the host plant for carbon (e.g., arbuscular mycorrhiza), but some mycorrhizal types can also exist as saprophytes in others. The nature of the relationship between plants and mycorrhizal fungi is mutual, but can also tilt in favor of the plant or the fungus depending on the environmental conditions and plant growth stage (Newton et al. 2010; Ryan and Graham 2018; Field et al. 2020). The mycorrhizal fungi benefit plants by improving their nutrient and water uptake and protect plants from different types of abiotic and biotic stresses (Smith and Read 2008; Lakshmipathy et al. 2019). Also, mycorrhizal fungi can have an important role in assisting interplant nutrient and signal transfer among plants in vegetation and in improving soil structure and quality through aggregation. In addition to their direct interaction with plants and soil, the mycorrhizal fungi also establish an intricate relation with a wide range of microorganisms in the soil (Hestrin et al. 2019). An understanding of the functionality of mycorrhizal symbiosis, their interaction with other microorganisms, and ecosystem processes is essential for the efficient use of the symbiosis for plant and habitat restoration and conservation (Pickles et al. 2020). The interaction between the mycorrhizal fungi and the host plant is diphasic with a part of the fungi within the root and the other in the soil. The part of the fungi that is present in the soil grows indefinitely beyond the nutrient depletion zone surrounding the roots exploring the soil for resources. These extraradical hyphae act as bridges in connecting the roots and the external soil environment. The intraradical phase of the mycorrhizal fungi transfers the nutrients taken up and translocated by the extraradical hyphae and also acquires and distributes the host-derived sugars and lipids to the soil hyphae. However, these functions and processes could be modified by the impact of other factors and modifying conditions. In this chapter, we first discuss the two major types of mycorrhizal symbiosis (arbuscular and ecto), and then the rhizosphere, hyphosphere, and the mycorrhizosphere. The reason for concentrating on arbuscular and ectomycorrhizal (EcM) types is that these mycorrhizal types are abundant in many natural and manmade ecosystems worldwide, occurring in 73% of the examined plant species (Brundrett and Tedersoo 2018). Moreover, these two mycorrhizal groups are well studied than others and are of application significance than the other mycorrhizal types. Furthermore, some ectomycorrhizal (EcM) trees like Picea abies and Pinus sylvestris are arbuscular mycorrhizal (AM) when they are young and later shift to EcM symbiosis (Kothe and Turnau 2018) while others like the eucalyptus, Alnus, and casuarinas are AM and/or EcM depending on environmental conditions.

2.2

Major Mycorrhizal Types

2.2.1

Arbuscular Mycorrhiza

Arbuscular mycorrhizal symbiosis is formed by fungi belonging to Glomeromycotina and Mucoromycotina of the phylum Mucoromycota (Spatafora et al. 2016). AM association is characterized by the presence of short-lived

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arbuscules that are formed in the root cortical cells and act as transit points for the transfer of nutrients to the plants. The AM symbiosis formed by taxa in Mucoromycotina is termed as fine root endophyte (FRE) owing to the fine nature of the fungal structures compared to those formed by members of Glomeromycotina. The fungus enters the roots directly or after forming an appressorium on the root surface. The penetrating hyphae coils in the first few cells and then ramifies the root cortex inter- and/or intracellularly. The intraradical hyphae can be either linear or coiled and different types of AM morphologies are recognized based on the type and distribution of the fungal structures within roots. Though Arum and Paris type of AM colonization were recognized in many plant species, a closer look at the AM colonization pattern in roots of several plant species revealed a large number of variants within them and is termed as intermediate types (Dickson 2004; Dickson et al. 2007). The diameter of the intraradical hyphae can vary with the associating fungi. For example, FRE produces much finer hyphae (3 μm). In addition to these intraradical structures, fungal storage structures that are rich in lipids called vesicles also occur in the colonized roots. Nevertheless, intraradical vesicles are not formed by fungi belonging to Gigasporaceae of Diversisporales and these fungi form vesicle-like structures called auxiliary cells in the soil. In FRE, terminal or intercalary hyphal swellings resembling vesicles are formed on the intraradical hyphae. The intraradical mycelium can extend into the soil forming an extensive network increasing the root surface area and connecting roots of coexisting plants in a plant community. The extraradical mycelium can reach 25 m/g of soil or more and exhibit great plasticity in exploiting the soil resources that are inaccessible to plant roots and act as a niche for diverse microorganisms (Lebrón et al. 2012; Jansa et al. 2013; Leyva-Morales et al. 2019). The extraradical mycelium of AM fungi can bear spores that act as chief perennating structures in seasonal vegetations. But, some species of AM fungi can also produce spores within plant roots.

2.2.2

Ectomycorrhiza

In EcM symbiosis, more than 20,000 fungi belonging to Ascomycetes, Basidiomycetes, and Zygomycetes establish symbiosis with approximately 6000 woody gymnospermous and angiospermous tree species (Kumar and Atri 2018). This symbiosis has a significant influence on the functioning of forest ecosystems, especially in the subtropical, boreal, and temperate regions where most of the component trees are colonized by EcM fungi (Mello and Balestrini 2018). In these ecosystems, the fungal mycelium of different EcM fungi can constitute up to 30% of the soil microbial biomass and interconnects a wide range of plant root systems, and these extramatrical networks are popularly known as the wood-wide web. The EcM association is defined by the occurrence of a fungal mantle that sheaths the host root and a Hartig net that envelops the rhizodermis and the cortical cells. The Hartig net presents a large surface area for the exchange of resources between the symbionts. The hormonal interaction between the plant and EcM fungi substantially alters the

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root architecture of the host plant that includes the development of short roots and inhibition of root hair formation (Kumar and Atri 2018). The EcM fungal hyphae may sometimes combine to form macroscopic structures termed as rhizomorphs that connect the sporocarps and aid in the acquisition of water (Johnson and Gehring 2007). The extraradical mycelial network of EcM fungi is much more extensive when compared to AM fungi and constitutes around 200 m of hyphae/gram of soil with a growth rate of 2–8 mm/day (Read and Boyd 1986; Ekblad et al. 2013). Like AM fungi, EcM fungi also occupy two niches: the host root and the soil. The EcM fungi access the soil for minerals, effectively take them through their extraradical hyphal network, and partly transfer it to the host roots. Although saprophytic, EcM fungi have lost a significant part of the capacity to decompose organic matter (OM) rich in lignocellulose (Martin et al. 2016). The adaptation of the EcM fungi to a symbiotic lifestyle though resulted in the loss of certain functions, but still, the fungus has acquired some mechanisms adopted by the biotrophic phytopathogens to colonize host roots and obtain sugars. However, the EcM symbiosis lacks specific morphological structures like the haustorium of phytopathogens to acquire host resources (Kumar and Atri 2018).

2.3

Rhizosphere

2.3.1

Soil as a Natural Support for All Living Organisms

Soil is a heterogeneous enriched medium that shelters many organisms and acts as solid physical support for plants (Farley and Fitter 1999). Microorganisms are important in regulating the functioning of soil nutrient cycling, structure formation, and plant interactions, both positively and negatively. Moreover, in both managed and natural soils, microorganisms participate in the critical processing of decomposition of OM, toxin removal, and the cycling of carbon, nitrogen (N), phosphorus (P), and sulfur (Garcia and Kao-Kniffin 2018). Soil aggregation is a biogeochemical and physical process in cultivated and bulk soils. The penetration and existence of fungal mycelial networks in plant roots and their interactions with soil enrich the soil ecosystem. Such long-term interactions allow the mycorrhizal mycelium to deposit a special type of protein called glomalin in the soil. Glomalin is an insoluble glycoprotein that glues the nearby soil particles and forms soil aggregates. The recommended method of extracting this glomalin as well as glomalin-related soil protein (GRSP) is done at 121
C in citrate buffer and quantified by Bradford assay as described by Rillig (2004). There are two fractions of glomalin, i.e., total glomalin and easily extractable glomalin (EEG). The occurrence of glomalin is strongly correlated with improved soil aeration, proper water drainage, enhancing soil carbon sequestration, and promoting microbial activity (Lovelock et al. 2004; Rillig 2004). Sumathi (2010) quantified influence of inoculation of Curcuma longa with Trichoderma sp., and other plant growth-promoting rhizobacteria (PGPR) on AM fungal colonization and EEG in soils. The results of the study indicated that inoculation with PGPR like Azospirillum, Pseudomonas sp.,

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and phosphate-solubilizing bacteria (PSB) enhanced the production of EEG fractions in the rhizosphere and AM fungal colonization in turmeric roots. This indicates that microbial inoculum in the soil significantly supports the biochemical activities of AM fungi and its contribution to nutrient cycling and plant nutrition. Glomalin is a form of OM that could engage in the sequestration of nitrogen and phosphate. This is evidenced by the existence of a strong correlation between plant protein concentration and EEG (Sumathi 2010). This relation between plant protein and EEG may be due to the translocation of phosphate and carbon that are necessary for the synthesis of proteins by the AM fungal hyphae (Miller and Jastrow 2000). These were also evidenced in a later study where the application of PGPR increased the AM fungal colonization levels in turmeric roots and OM content of the soil (Sumathi et al. 2013). The AM fungal hyphae that are trapped in the soil aggregates undergo a slow decomposition process, having an estimated residence time of 6–42 years (Rillig 2004). Glomalin production significantly reduces the turnover of the AM fungal hyphae. The soil aggregates represent more the 5% of total soil carbon, significantly contributing to long-term soil carbon sequestration (Wright and Upadhyaya 1998; Rillig et al. 2001). Although the actual factors that control glomalin production are still unknown, factors like soil type, climate, AM fungal species involved, host plant, and their productivity are presumed to contribute to the concentrations of glomalin in the soil (Sumathi et al. 2013).

2.3.2

Difference Between Rhizosphere and Non-Rhizosphere

Hiltner (1904) defined the rhizosphere region as the soil in the root-zone area with interactions of microorganisms. The rhizosphere region supports a large group of living organisms than bulk soils. Diverse microorganisms ranging from unicellular to multicellular and macroscopic organisms survive in the rhizosphere environment. The colonization of microorganisms in the rhizosphere is induced by the activity of plant roots. Many microorganisms are attracted toward the nutrients released by the plant roots. The exudates from the plant roots called “rhizodeposits” contain a variety of low-molecular-weight molecules like small amino acids, glucose, fatty acids, and organic acids and high-molecular-weight molecules like polysaccharides and polygalactic acids. Some molecules present in the exudates may act as signal molecules to initiate colonization of roots by microorganisms. Root exudation activates “rhizosphere priming,” which is an increased rate of microbial-mediated decomposition of the OM in the soil (Kuzyakov 2002). The liberation of low-molecular-weight carbon compounds into the rhizosphere by plant roots induces the saprophytic microbes in the soil to produce extracellular enzymes that mediate the breakdown of high-molecular-weight organic compounds. This results in the liberation of labile inorganic and organic nutrients available to both plants and soil microorganisms. Plant and microbe interaction in the rhizosphere takes place following various principles and mechanisms that may be either beneficial or harmful. Plants attract

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root colonizing microorganisms through a chemical signaling process known as chemotaxis. Further, most of the plants behave as obligate mycotrophs as they have the ability to induce germination of mycorrhizal spores present in the soil and to attract the germinating hyphae (Vierheilig et al. 1998). Non-rhizosphere soils are not influenced by plant roots and therefore are characterized by low fertility as well as the diversity and abundance of microorganisms (Li et al. 2016; Olahan et al. 2016). However, non-rhizosphere soil is essential for the soil aggregate stability and resistance of the soil to nutrient leaching and soil erosion (Elbl and Záhora 2014). Long-term monoculture of black pepper is known to considerably increase the relative abundance of Acidobacteria in the non-rhizosphere, and contrarily the abundance of Bacteroidetes and Firmicutes tended to decrease (Li et al. 2016). Nevertheless, populations of certain microorganisms appear to be similar in both rhizosphere and non-rhizosphere regions. For example, populations of the pathogenic fungus Fusarium has been shown to increase both in the rhizosphere and non-rhizosphere soils with time thereby increasing the incidence of wilt in both the soil regions (Li et al. 2016). Cropping patterns could also substantially affect the microbial diversity in the non-rhizosphere soils. Continuous cropping of ginseng both in the understory wild and farmlands decreased the operational taxonomic unit (OTU) richness of fungal communities in the non-rhizosphere soils (Bao et al. 2020). In addition, changes in microbial communities in response to the season also tend to vary in the rhizosphere and non-rhizosphere regions. An analysis of the seasonal changes in bacteria and fungi in the rhizosphere and non-rhizosphere regions of Camellia yuhsienensis over a one-year period indicated different responses in the soil regions. The abundance and changes in OTUs were higher in the rhizosphere region than in the non-rhizosphere region for both fungi and bacteria (Li et al. 2020).

2.3.3

Microbial Interactions

Apart from the mycorrhizal symbiosis, other microorganisms also form mutual relationships not only with plants but also with the associating fungi forming multitrophic interactions (Bonfante and Anca 2009). For instance, a non-culturable Gram-negative bacterium Glomeribacter gigasporum, a taxon of Burkholderiaceae, lives as an endosymbiont in the spore vacuoles, intraradical mycelium, and hyphae of AM fungi Gigaspora margarita. Similarly, some rhizobacteria belonging to Bacillus, Paenibacillus, and Pseudomonas frequently associate with AM fungi. The PGPR in the soil ecosystem also form symbiotic associations with plant roots. These rhizobacteria stimulate the development of AM fungal mycelium and spore germination as well as plant root colonization (Barea et al. 1998). Microorganisms associated with plants improve nutrient acquisition by roots and stimulates hormone production. The PGPR perform various beneficial activities, in particular nitrogen fixation, phosphate solubilization, and suppression of plant pathogens (Martínez-Viveros et al. 2010). The well-studied plant growth supporting bacterial genera are Rhizobium, Azospirillum, Bacillus, Pseudomonas, and Serratia.

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Plant-associated bacteria and fungi confer direct support for plant growth simultaneously inhibiting plant pathogens (Thakore 2006). The mycorrhizal colonization brings diverse changes in the plant root architecture and physiology, as well as enriches the quality and quantity of root exudates. The changes in root exudation pattern occur when plant roots are colonized by AM fungi. The rhizosphere is extended by the extraradical mycelium of the AM fungi that explores the bulk soil for resources. The fungal hyphae also exude carbon and the region of the soil influenced by the fungal hyphae is called hyphosphere. This soil region also supports special microbial communities like the rhizosphere. The activation of plant defense mechanisms against specific target pathogens is an important criterion to use AM fungi as biofertilizer. The interaction between plant-parasitic nematodes and AM fungi is reported to be opportunistic. The biocontrol activity of AM fungi is also an added advantage of AM fungi–plant symbiosis, which supports increased plant growth and deters or decreases the damages caused by plant pathogens.

2.4

Mycorrhizosphere

The soil region encompassing the rhizosphere and the hyphosphere is called the mycorrhizosphere (Jeffries and Barca 2012) (Fig. 2.1). The influence of AM fungi and the plant root systems on the microbial communities and nutrients in the soil is known as the mycorrhizosphere effect. Angelo Rambelli in 1973 shaped the concept of mycorrhizosphere to indicate soil microhabitat that was influenced by the metabolites exudated by the roots and its associated mycobiont (Rambelli 1973). The intimate interaction of the associating fungi with the plant root system renders the mycorrhizosphere more complex than the root-influenced rhizosphere (Voronina 2009; Voronina and Sidorova 2017). Therefore, this region is not only influenced by the roots but also by the associated symbiont. Previous studies have explored only the interaction and benefits between the plants and their associated symbiotic fungi. However, the role of mycorrhizosphere microbiota was later perceived with the evolution of the multitrophic concept in mycorrhization and great advancements in research techniques (Voronina et al. 2011; Voronina and Sidorova 2017). In addition Fig. 2.1 Diagrammatic representation of the mycorrhizosphere concept

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to the extraradical hyphal networks in the soil, the intraradical phase of the mycorrhizal fungi can also shape the microbiota in the mycorrhizosphere. This stems from the fact that colonization of roots by mycorrhizal fungi has been shown to modify the quality and quantity of root exudates (Vives-Peris et al. 2020). The establishment of the functional mycorrhizosphere is dependent on the successful establishment of the symbiosis between the plants and the associating fungi. The primary step in this process is the maintenance, growth, and survival of AM fungal spores in the soil and stimulation of mycelium development for pre-symbiotic growth. In addition to the plant signals, bacteria present in the mycorrhizosphere are also known to play a pivotal role in the establishment of symbiosis both by AM and EcM fungi. Roesti et al. (2005) showed that the bacterial communities associated with the spores Funneliformis geosporus (¼Glomus geosporum) and Septoglomus constrictum (¼Glomus constrictum) are more dependent on fungal identity than the host plant identity. Moreover, it was also suggested that the composition of the bacterial communities associated with spores of the AM fungi could be greatly influenced by the spore wall composition or the exudate of the fungi rather than by the root exudates of the host plant. A scanning electron microscopic observation of the F. geosporus spores showed that the bacteria colonizing the spore surface was presumably feeding on the outer layer of the spore wall and it was speculated that the activity of the spore surface bacteria could benefit the process of spore maturation and its eventual germination (Roesti et al. 2005). Moreover, in plants, the associating bacteria also increase the susceptibility of roots for mycorrhizal colonization and simultaneously induce root to recognize mycelium. Finally, it also modifies the physicochemical properties of the soil that would benefit mycorrhiza formation.

2.4.1

Mycorrhiza Helper Bacteria

The group of soil bacteria supporting the formation of mycorrhizal symbiosis with plants is called “helper bacteria” or “mycorrhiza helper bacteria” (MHB). The first association of MHB with endomycorrhizal fungi was reported by Mosse (1962). Both Gram-positive and Gram-negative bacteria act as MHB. The bacterial genera reported functioning as MHB includes Agrobacterium, Azospirillum, Azotobacter, Pseudomonas, Bacillus, Burkholderia, Bradyrhizobium, Enterobacter, Klebsiella, Rhizobium, and others of which Pseudomonas tends to be the dominant genus. The Actinomycetes Rhodococcus, Streptomyces, and Arthrobacter can also act as MHB. The fungus Trichoderma harzianum was also found to enhance AM fungal colonization and hence Jayanthi et al. (2003) suggested the term to be changed as “mycorrhiza helper organisms” to accommodate bacteria, fungi, or any other enhancing mycorrhizal symbiosis, which was not followed by many later workers. The constructive effect of MHB on mycorrhizal–host plant symbiosis depends on root sensitivity and stimulation of spore germination (Xavier and Germida 2003; Frey Klett et al. 2007). A direct beneficial aspect of MHB involves the stimulation of plant growth and indirect benefit includes inhibition of pathogen growth or a reduction in the adverse effects of phytopathogens on plants (Hernandez Montiel

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et al. 2013; Deveau and Labbé 2016). The abundance of the bacteria can vary in the hyphosphere. Some bacteria attach to the fungal hyphae and stimulate the production of hyphal exudates while others mediate the adhesion of other bacteria or some of them can form biofilm on the hyphoplane (Haq et al. 2014). MHB benefits plant nutrition by being an N-fixing rhizobacteria (Paul and Lade 2014). Additionally, they interfere directly with the immune response of the plant by activating several pathways like jasmonic acid and salicylic acid (Cameron et al. 2013; Kurth et al. 2013). Some species of MHB are known to produce hormones like auxins and ethylene that modulate root development (Vacheron et al. 2013). The bacterial gene operons containing Type III Secretion System (T3SS) are enriched at the surrounding area of mycorrhizal fungi. T3SS functions as injecting systems of bacteria to deliver small effector molecules into plant root nuclei to induce some functions. T3SS is related to formation of both symbiotic and pathogenic associations. Still, the mechanisms of injections by bacteria into eukaryotic cells are not clearly understood (Warmink and van Elsas 2008; Viollet et al. 2011).

2.4.2

Interactions of Mycorrhizal Fungi with Beneficial Microflora

The microorganisms existing in the mycorrhizosphere region exert valuable effects on plants as well as other symbiotic microorganisms. When such microorganisms positively influence the growth of plants, they are designated as plant growthpromoting microorganisms (PGPM). The bacteria surviving in the roots’ rhizospheric region are called rhizobacteria and those supporting plants’ development or metabolism are considered PGPR. The term PGPR was coined by Kloepper and Schroth (1978). The PGPR stimulates plant growth either through direct or indirect mechanisms (Bashan and Holguin 1998). In the rhizosphere, the presence of Funneliformis mosseae enhances the population load of Pseudomonas fluorescens, which exhibits plant growth-promoting effect (Edwards et al. 1998). Nitrogen is the most important nutrient necessary for plant growth. The molecular nitrogen (N2) available in the atmosphere (78%) is in the gaseous form and should be converted to the chemical form of ammonia (NH3) that can be utilized by the plants. This simple reduction process is carried out by bacteria capable of producing the enzyme “nitrogenase” (Olivares et al. 2013; de Bruijn 2015). Nitrogen fixation can be possible either by artificial or natural means; the natural way is quite costeffective. This particular process is carried out by free-living and symbiotic bacteria. The symbiotic bacteria include Rhizobium and Frankia. For instance, the bacterial genus Azospirillum, which is known to fix atmospheric N, forms an associative association with plant roots. The free-living bacteria Azotobacter, Klebsiella, and Bacillus are known to fix nitrogen in the soil. The soil bacteria and fungi participate in the breakdown of organic substrates and release nutrients into the soil environment. This process is known as mineralization. Phosphorus mineralization releases orthophosphates from organic phosphates into the soil (Marschner 2008; Richardson et al. 2009; Bagyaraj et al. 2015). For instance, bacteria and fungi belonging to Bacillus, Pseudomonas, Aspergillus, and Penicillium

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carry P mineralization in the soil. Mineralization is carried out by the non-specific activity of phosphatase enzymes (including acid and alkaline phosphatases). These phytase enzymes act specifically on phytates to release orthophosphates. P release by microbial activity enhances plant growth. If mycorrhizal fungal hyphae are present in this habitat, it effectively absorbs the P nutrients and transfers them to plant roots (Richardson et al. 2009). The evidence for this symbiotic association is given by Koide and Mosse (2004). Certain studies have shown that the EcM can modulate the composition of the bacterial communities associated with the mycorrhizospheres. Shirakawa et al. (2019) examined the influence of EcM fungal species associated with Pinus densiflora on cultural bacterial communities in the mycorrhizosphere. The results of the study indicated that Gram-positive bacteria are excluded from the mycorrhizosphere of P. densiflora due to the antibacterial activity of the EcM fungi. Moreover, increased diversity of plant genotypes has been shown to alter the root competition and the levels of EcM and endophyte fungal colonization in the mycorrhizosphere (Baum et al. 2018). Several studies have shown that EcM roots can significantly influence the archaea and bacterial community composition in forest soils (Fransson and Rosling 2014; Rinta-Kanto and Timonen 2020). An investigation on the impact of the EcM fungi Tuber panzhihuanense in symbioses with Corylus avellana suggested a high diversity in microbial communities during the initial stages of symbiosis development (Yang et al. 2019). Moreover, the structure of the bacterial and fungal communities associated with C. avellana was completely different in the presence and absence of the EcM symbiosis. Certain bacteria like Herbiconiux, Pedomicrobium, and Rhizobium, and the fungal taxa Monographella were more prolific in the presence of EcM symbiosis (Yang et al. 2019). A culture-independent analysis of the bacterial and archaeal populations associated with the mycorrhizospheres of Pinus sylvestris–Suillus bovinus in a boreal forest of Finland indicated that archaea dominated by Thaumarchaeota taxa were more abundant than the bacterial taxa dominated by Acidobacteria, Actinobacteria, and Proteobacteria (Rinta-Kanto and Timonen 2020). Further, a higher prokaryotic population was associated with the soil hyphae of S. bovinus than in the roots. Some of the factors that contribute to the variation in the prokaryotic population in EcM could be root age, mycorrhizal, and soil hyphal abundance. Though bacterial communities associated with EcM roots tend to stabilize with time, significant variability in bacterial communities has been noted during the early stages of colonization and symbiosis establishment (Marupakula et al. 2016). In a recent study, Gorka et al. (2019) showed that the EcM hyphae could accelerate the transfer of host-derived carbon to bacterial communities far away from roots and this carbon transfer was associated with the changes in the soil nutrients. These results clearly indicate that the EcM symbiosis could modify the microbial communities associated with their host plant in addition to their influence on soil factors.

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Interactions of Mycorrhizae with Pathogenic Microorganisms

Mycorrhizae are involved in effective disease control mechanisms. The popular AM fungus F. mosseae increased the population of PGPR particularly P. fluorescens in the rhizosphere soil (Edwards et al. 1998). Among bacteria, Pseudomonas and Bacillus are the potent candidates for biocontrol agents. A combination of mycorrhizae and rhizobacteria associated with plants develops resistance against fungal pathogens (Paulitz and Linderman 1991). Pathogens make entry into the host cells and induce disease symptoms. Further, the symptoms are regulated by the colonization of AM fungi in the host plant and induce the immune response (Induced Systemic Resistance—ISR) against plant pathogenic microorganisms (Liasu and Shosanya 2007). Various compounds are found associated with ISR including enzymes like superoxide dismutase (SOD), chitinases, chitosanases, and peroxidases and specific proteins like pathogenesis-related type-1 proteins (PR-1 proteins). The accumulation of molecules like phenolics and jasmonic acid indicates the disease resistance nature of plants. The effectiveness of endomycorrhizae to control soilborne fungal pathogens is due to their efficiency to induce rhizobacteria against suitable factors supporting pathogen in the mycorrhizosphere. AM fungi confer biocontrol activity against pathogens inducing systemic and local resistance mechanisms (Toussaint et al. 2008). ISR increases the density of the plant cell wall and thus restricts the phytopathogens to the outer root cortex (Benhamou et al. 1998). Inoculation of AM fungi prevents the attack of pathogens and confers protection for the plants (Singh et al. 2010; Bagyaraj 2018). Mycorrhizosphere creates a safe environment by decreasing the growth of nematodes and reducing the incidence of conidial formation by Fusarium oxysporum f. sp. chrysanthemi. The colonization of tomato plant roots with Rhizophagus intraradices (¼Glomus intraradices) reduces the growth and root rot symptoms of Fusarium solani f. sp. phaseoli (Akköprü and Demir 2005). The biocontrol potential of AM fungi resides in the competitive environment with the soil fungal pathogens for space and nutrients. The combined inoculation of R. intraradices and bacteria Pseudomonas striata and Rhizobium sp. significantly reduced the gall formation and population development of nematode in chickpea (Akhtar and Siddiqui 2008). Like AM fungi, ectomycorrhizal association also protects its host plants from various diseases. Osaki-Oka et al. (2019) showed that the volatile extracts of the EcM fungi Russula aff. anthracina, Russula chloroides, and Russula senecis inhibited the conidial germination of the phytopathogenic fungus Alternaria brassicicola. Similarly, inoculation of Pinus tabulaeformis seedlings with seven EcM fungi (Suillus lactifluus, Suillus bovinus, Suillus tomentosus, Handkea utriformis, Amanita vaginata, Suillus laricinus, and Schizophyllum sp.) reduced the mortality and improved the seedling growth and root architecture against the pine wilt disease caused by the nematode Bursaphelenchus xylophilus (Chu et al. 2019). In a recent study, Chartier-Fitz Gerald et al. (2020) showed that the EcM fungal (Lactarius quieticolor, Suillus granulatus, and a Suillus sp.) inoculation improved the seedling growth and afforded protection against the fungal pathogen

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Fusarium circinatum. Studies have also shown that the EcM can modulate the susceptibility of the host plants variedly against different pathogens. For instance, association with the EcM fungus Suillus luteus decreased the susceptibility of P. sylvestris to the fungal pathogen Heterobasidion irregulare, but not against Heterobasidion annosum (Gonthier et al. 2019).

2.4.4

Interactions of Mycorrhizae with the Stressed Soil Environment

Soil acts as a substrate for growth and reproduction of microorganisms and other small living communities. These organisms actively participate in the conversion of complex organic molecules into simpler substances that can be easily absorbed by plant roots and other organisms. Different types of pollutants are introduced into soils due to various anthropogenic activities and many of these soil pollutants rarely undergo the degradation process. One of the most common and widespread pollutant added to the soil are the heavy metals. These pollutants are brought into the soil environment by human activities like industries, metal plating, electronic wastes, and petroleum products. Moreover, agricultural activities like the use of pesticides, agrochemicals, phosphatic fertilizers, and sewage sludges for irrigation also add a higher concentration of heavy metals into the soil environment. Heavy metal pollution causes drastic health defects in plants, animals, and humans. Microorganisms are capable of detoxifying the toxic heavy metal pollutants. Among different types of microorganisms, mycorrhizal fungi are efficient candidates for detoxifying soil pollutants and protecting plants from these toxic chemicals (Sumathi 2010). Nevertheless, heavy metals can influence the formation and functioning of AM fungi. An excessive concentration of heavy metals can reduce the spore number and germination, hyphal length, and percentage of colonization of AM fungi (Krishnamoorthy et al. 2019). In addition, heavy metals can have a harsh impact on the ecology and diversity of AM fungi. Several mechanisms are associated with AM fungi in imparting tolerance to heavy metals in plants, which have been reviewed in detail by Riaz et al. (2020). Release of the glomalin protein by mycorrhizal hyphae into the soil is one of the most important mechanisms for the amelioration of heavy metal toxicity. Other processes involved in heavy metal tolerance involve extracellular chelation, binding, and accumulation of heavy metals in cell walls of spores and hyphae (Krishnamoorthy et al. 2019). The vesicles and spores of AM fungi act as storage structures of heavy metals. This reduces the availability of heavy metals in the rhizosphere or mycorrhizosphere. The AM fungi also absorb and transfer the metal ions from the soil to plant roots that are then translocated to the aerial parts of plants. The glomalin protein eases the uptake of water, and improves the soil structure by increasing the water holding capacity, gaseous exchange, and availability of water and nutrient both in stressed and normal soils. Glomalin also reduces the bioavailability of metal ions and participates in indirect mechanisms for increased water and nutrient uptake, particularly P acquisition through hyphae, mediating the

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growing of plants in heavy metal stressed soils (Garg and Bhandari 2012; Garg and Chandel 2015). The influence of an AM fungus Rhizophagus irregularis and an EcM fungus Sphaerosporella brunnea inoculation either individually or in combination on growth and trace element extraction was examined in Salix miyabeana (clone SX67) on an industrial landfill that was decommissioned several decades back in Canada (Dagher et al. 2020). Salix plants inoculated with S. brunnea accumulated the highest biomass after two growing seasons. Contrarily, the inoculation of R. irregularis either alone or along with EcM failed to significantly influence the plant biomass and the trace element extraction. Inoculation of S. brunnea also significantly decreased the concentrations of copper, lead, and tin in the soil (Dagher et al. 2020). The MHB also accompanies the mycorrhizal fungi in detoxifying the toxic compounds present in the soil (Duponnois and Garbaye 1990). Remediation of xenobiotic compounds using the rhizosphere processes associated with plants is also called phytostimulation. The xenobiotic compounds are detoxified by the multitrophic activities in the mycorrhizosphere that acts as a remediation unit in the ecosystem (Bhawana and Fulekar 2011).

2.5

Perspectives of Mycorrhizosphere for Sustainable Agriculture

Managing mycorrhizosphere interactions (mycorrhizosphere tailoring), involving co-inoculation with selected AM fungi and other beneficial microorganisms like N-fixers, P-solubilizers, and PGPR, is recognized as a possible biotechnological tool to improve the growth and productivity of crop plants in sustainable agriculture. It is fundamental that the establishment of mycorrhizosphere-tailored plants increases soil nutrient content and improves other physicochemical properties, which define soil quality promoting plant growth. Some studies also brought out that tailored mycorrhizosphere improved plants’ survival, growth, and out-planting performance under biotic and abiotic stress conditions (Azcon-Aguilar and Barea 2015; Karthikeyan et al. 2016). Further, few studies revealed that mycorrhizospheretailored plants act as an inoculum resource for other crops/surrounding vegetation grown under inter/mixed cropping systems. Most of the mycorrhizosphere studies have been done under pot culture conditions. Evaluation of such inoculation studies under field conditions is rather limited. Studies on mycorrhizosphere tailoring, improving growth, nutrition, and yield of crop plants, and also the possibility of reducing chemical fertilizer input, thus upholding the theme of sustainable agriculture, are discussed briefly hereunder.

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Mycorrhizosphere Tailoring with AM Fungi and N-Fixers

Janse (1896) was the first to describe the interaction between AM fungi and rhizobia in the legume Pithecellobium montanum. The early field experiments conducted with Medicago sativa by Azcón-Aguilar et al. (1979) and soybean by Bagyaraj et al. (1979) under field conditions clearly brought out that dual inoculation with AM fungi and rhizobia shows a synergistic effect in improving nodulation and AM fungi colonization consequently enhancing growth, nutrition, and yield compared to single inoculation and uninoculated plants. This was followed by similar reports in other legumes. Several studies on the interaction between AM fungi and symbiotic N-fixing organisms suggest that the interaction is synergistic, improved nodulation and N-fixation by N-fixers, and N-fixers enhanced colonization and P uptake by AM fungi; thus dual inoculation improves plant growth much better than single inoculation with either of them (Meena et al. 2018). It is well known that N-fixation has a high phosphate requirement, which is provided by AM fungi. Extracellular polysaccharides and dehydrins produced by rhizobia enhancing colonization by AM fungi have been observed. The response of cowpea and pigeon pea to dual inoculation with AM fungi Rhizophagus fasciculatus (¼Glomus fasciculatum) and Rhizobium sp. with and without added P (22 kg P ha1) was studied in a P-deficient soil. Plants inoculated with both the organisms and supplemented with P recorded the highest shoot dry weight, and N and P contents, indicating the need for the addition of a small amount of P to derive maximum benefit from dual inoculation with AM fungi + rhizobia (Manjunath and Bagyaraj 1984). Almost similar observations were also reported in the tree legume Leucaena leucocephala inoculated with R. fasciculatus and rhizobia (Manjunath et al. 1984). Another co-inoculation study with AM fungi + rhizobia done with soybean genotypes brought out that deep-rooted genotype benefitted more from co-inoculation than shallow-rooted genotype. The improvement in plant growth parameters was more prominent in low fertile soil (Wang et al. 2011). Another study demonstrated that combined inoculation of chickpea with F. mosseae + Rhizobium ciceri with a split application of N fertilizer significantly increased the yield and quality of the grain compared to inoculation with any one of the inoculant (Malekian et al. 2019). Meng et al. (2015) investigated inoculation with F. mosseae and Rhizobium japonicum in maize/soybean intercropping system. Inoculation improved the N-fixation efficiency of soybean and promoted N transfer from soybean to maize, resulting in improvement of yield in both the crops. Raklami et al. (2019) studying the interaction among AM fungi + rhizobia + PGPR in Vicia faba under field conditions reported synergistic interaction between the three organisms, resulting in improved growth, nutrition, and yield of the crop. Certain conclusions that can be drawn from the experiments done so far are, to screen and select the best AM fungi and rhizobia for the target legume, and then study the interaction between the two selected symbionts under polyhouse and finally under field conditions. Another conclusion drawn is that the tripartite symbiosis is not effective in soils with high levels of N and P (Barea et al. 2014). Clearly, mycorrhizosphere interactions in legume plants have a

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relevant significance on N and P cycling in the biosphere to benefit sustainable agriculture. Synergistic interaction between AM fungi and free-living N-fixing Azotobacter was reported for the first time by Bagyaraj and Menge (1978). This was confirmed by later studies by many workers as outlined in the review by Karthikeyan et al. (2016). Amirnia et al. (2019) carried out field experiments with R. intraradices and Azotobacter sp. inoculation to lentil under rainfed and irrigated conditions. Under both conditions, dual inoculation increased the biomass, yield, and seed protein concentration. The benefit of inoculation was much higher under irrigated conditions. In another study conducted at Desert Research Centre, Egypt, with AM fungi and Azotobacter inoculation under four water regimes brought out that dual inoculation significantly enhanced yield attributes and water use efficiency of barley compared to single inoculation with either of them (Abdelhameid and Kenawey 2019). Kumar et al. (2016) evaluated the effect of AM fungi consortia and Azotobacter sp. on Jatropha curcas under field conditions in a semi-arid region. A significant improvement in plant growth and fruit yield was evident when AM fungi and Azotobacter were co-inoculated.

2.5.2

Mycorrhizosphere Tailoring with AM Fungi and P-Solubilizers

Studies on dual inoculation with AM fungi and phosphate-solubilizing microorganisms (PSM) brought out increased plant growth and yield compared to single inoculation with either of them. This is because P solubilizers solubilize and release H2PO4 ions from unavailable forms of P and AM fungi help in the uptake of H2PO4 ions from soil (Aliasgharzad et al. 2009; Bagyaraj et al. 2015). Some workers found that PSM inoculated onto seeds or seedlings maintained high populations, longer in the rhizosphere of mycorrhizal than non-mycorrhizal roots. Combined inoculation of PSM with AM fungi along with rock phosphate could improve crop yield in nutrient-deficient soils (Sabannavar and Lakshman 2009). Synergistic interactions between AM fungi and PSM with consequential benefit on plant growth have been demonstrated not only in crop plants but also in forest trees (Adesemoye et al. 2008). Interaction between the AM fungus Rhizoglomus irregulare and PSM Pseudomonas putida was studied in an intensive maize agricultural system. The results clearly showed that dual inoculation increased maize productivity and at the same time improved P use efficiency (Pacheco et al. 2020). In calcareous soils low availability of P is a major problem because of precipitation of P by calcium, thus making it immobile. Maize crop was inoculated with AM fungi + PSM and treated with rock phosphate in the first season. In the next season, wheat crop was taken as a subsequent crop to check the residual effect of inoculation. The results of both the field trials indicated the beneficial effect of dual inoculation in increasing grain yield and P uptake, suggesting the replacement of expensive P fertilizer in P-deficient calcareous soils (Wahid et al. 2020). Field studies have shown that inoculation with efficient AM fungi not only increases the growth and yield of crop plants but also reduces the application of

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phosphatic fertilizer by nearly 50%, especially in marginal soils deficient in nutrients. Though the rock phosphates available in India are of low grade and not fit for the manufacture of phosphatic fertilizer, they can be used with PSM plus AM fungi as a potential source of P for crop plants, thus bringing down the import of P fertilizers/rock phosphate in our country. Some studies also revealed that the total cost of cultivation and the gross income, net profit per hectare, and the cost–benefit ratio are also high when AM fungi and PSM are inoculated together with rock phosphate under field conditions (Ajimuddin 2002).

2.5.3

Mycorrhizosphere Tailoring with AM Fungi and PGPR

Interaction studies carried out with AM fungi and PGPR also revealed enhanced plant growth and yield. The synergistic effect of PGPR and AM fungi on plant growth promotion is well documented (Bagyaraj 2014; Desai et al. 2016). The combined application of P. fluorescens and F. mosseae resulted in improved growth of chickpea compared to the application of the two bioinoculants separately and also reduced the galling and multiplication of the nematode pathogen Meloidogyne javanica (Siddiqui and Mahmood 2001). In combined inoculation of PGPR and AM fungi, PGPR stimulating spore germination and colonization of AM fungi and in turn better plant growth has also been reported (Desai et al. 2016). Synergistic interaction between Glomus bagyarajii and Trichoderma harzianum promoting growth and yield of Piper longum (Ulfath Jaiba et al. 2006) and that of chilli with F. mosseae and Bacillus sonorensis inoculation (Thilagar et al. 2014) has been reported. Another study brought out that co-inoculation of pigeon pea with Ambispora leptoticha (¼Glomus leptotichum) and Pseudomonas, and finger millet with R. fasciculatus and Pseudomonas as intercrop benefitted both the crops under field conditions in different agro-ecological locations (Mathimaran et al. 2018). Inoculation of neem with F. mosseae + Paenibacillus polymyxa improving the growth and nutrition of seedlings in the nursery and when planted in the field has been reported recently (Nikhil et al. 2020). In medicinal and aromatic plants, dual inoculation with AM fungi and PGPR enhanced not only growth and yield but also the secondary metabolite concentration of medicinal value, which has been reported by many workers. An increase in eugenol concentration in Ocimum sanctum (Jyothi and Bagyaraj 2017), with anolide concentration in Withania somnifera (Anuroopa and Bagyaraj 2017), and essential oil content in Ocimum basilicum and Satureja hortensis (Khalediyan et al. 2020), has been brought out by earlier workers. Field studies conducted with selected AM fungi and PGPR combination revealed that in addition to improved growth and yield of crop plant, application of chemical fertilizer can be reduced. Inoculation with F. mosseae + Trichoderma harzianum not only improved growth, P nutrition, and yield of Andrographis paniculata, but also helped in saving 25% of P fertilizer application (Arpana and Bagyaraj 2007). Application of Acaulospora laevis + Bacillus licheniformis enhanced the growth and yield of Withania somnifera and also reduced the application of NPK—fertilizers by 25% (Anuroopa et al. 2017). In Ocimum tenuiflorum treatment with Funneliformis

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monosporus (¼Glomus monosporum) + Pantoea dispersa and in chilli with F. mosseae + Bacillus sonorensis resulted in 50% saving of NPK fertilizer application (Thilagar et al. 2018; Jyothi and Bagyaraj 2018). Another study brought out that dual inoculation with the AM fungus R. fasciculatus and PGPR P. fluorescens was very effective in ameliorating the root rot and wilt disease of the medicinal plant Coleus forskohlii caused by Fusarium oxysporum (Rakshapal Singh et al. 2009). The production of good-quality seedlings that will establish better in the field is very much essential for crop productivity. Growing seedlings in pro trays is an innovative technique adopted in nurseries, including India, where seedlings are grown in soilless media under polyhouse conditions (Singh et al. 2017). Inoculating the substrate/seeds with selected AM fungi + PGPR has helped in the production of healthy vigorously growing seedlings that will perform better when planted in the field. Recent studies on inoculation with F. mosseae + Bacillus sonorensis resulted in vigorously growing seedlings of vegetable crops like tomato and capsicum (Abhaya et al. 2019; Desai et al. 2020), and flowering plants like zinnia and balsam (Sukeerthi et al. 2020).

2.5.4

Mycorrhizosphere Tailoring with Microbial Consortia

Studies have shown that inoculation with microbial consortia consisting of efficient AM fungi together with a N-fixer, P-solubilizer, and PGPR, carefully screened and selected for a particular crop or forest tree species, is more beneficial than AM fungi alone in improving the growth, biomass, and yield. Thus, the recent trend is to use microbial consortia of more than two microorganisms for inoculating crop plants and forest tree species, the consortia mostly consisting of one selected AM fungi with several selected PGPR. These studies have brought out clearly that inoculation with such microbial consortia is far superior to inoculating singly with any AM fungi or PGPR alone, or a combination of a single AM fungi + single PGPR. Few other studies brought out that such mycorrhizosphere tailoring with selected microbial consortia not only improves the growth and yield of crop plants but also saves the use of chemical fertilizers. Microbial consortia consisting of F. mosseae + Paenibacillus polymyxa + Pantoea agglomerans increased the growth and yield of French beans and also saved the application of NPK fertilizers by 50% (Hemlata and Bagyaraj 2015). Microbial consortia consisting of AM fungi Claroideoglomus etunicatum (¼Glomus etunicatum) + PGPR Azotobacter chroococcum + Trichoderma harzianum + Burkholderia cepacia in addition to increasing the yield and essential oil content of the aromatic crop Pogostemon cablin reduced the application of N and P fertilizer by 50% (Arpana et al. 2010). The performance of a selected microbial consortia Scutellospora calospora + Azotobacter chroococcum + Bacillus coagulans + T. harzianum on Acacia auriculiformis was evaluated through largescale nursery trials. The results showed a 31% increase in the dry biomass of inoculated seedlings compared to uninoculated seedlings. These seedlings when planted in the wasteland and monitored for six years showed a 52% higher

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biovolume index than that of the uninoculated trees (Raghu et al. 2020a). Similar results were obtained with Tectona grandis inoculated with microbial consortia Ambispora leptoticha + Azotobacter chroococcum + T. harzianum (Raghu et al. 2020b). Therefore, the need of the hour is to develop microbial consortia for inoculating different crop plants and the promotion of these consortia in the ecofriendly sustainable production of crop plants for the benefit of mankind. More field inoculation trials to exploit the benefit of tailored mycorrhizosphere enhancing crop productivity should be a component in sustainable agricultural strategies in the future, particularly in a world of depleting non-renewable resources. The mycorrhizosphere tailoring is likely to become even more importunate due to the agro-ecological threats of agrochemicals, which are urgently required to be reduced to increase food quality, sustainable food production, and environmental protection.

2.6

Conclusion

Generally, plants interact with a wide range of microorganisms either directly or indirectly. Some of the organisms like the mycorrhizal fungi that associate with roots benefit plants in various ways. This positive influence of mycorrhizal symbiosis is modulated by other organisms that are present in the rhizosphere and hyphosphere. Studies conducted so far clearly suggest that the mycorrhizosphere encompassing the spheres of the root and the associating fungal hyphae could influence the diversity of microorganisms and the soil characteristics. Therefore, this region of the soil is of great relevance in improving plant growth and health. Moreover, whatever evidences that are available on the various processes in the mycorrhizosphere are only the tip of an iceberg. There are several aspects like the factors that determine the discrimination of the rhizosphere, hyphosphere, and mycorrhizosphere as indicated by Voronina and Sidorova (2017). Furthermore, the exchange of signals between the different components of the mycorrhizosphere, stability, and succession of various microbial groups during the establishment and functioning of the mycorrhizosphere are yet to be ascertained. In addition, understanding the role of plant diversity on the mycorrhizosphere is important as plant roots in vegetation are connected through the common mycelial network. Therefore, untangling the complexity and dynamism of the mycorrhizosphere would greatly enable to increase the efficiency of the mycorrhizal symbiosis in sustainable crop production systems. This suggests the need for intensifying research on mycorrhizosphere tailoring for improving plant productivity under different agroecological conditions in the years to come.

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Conservation Strategies for Rhizobiome in Sustainable Agriculture Md. Mahtab Rashid, Basavaraj Teli, Gagan Kumar, Prerna Dobhal, Dhuni Lal Yadav, Saroj Belbase, Jai Singh Patel, Sudheer Kumar Yadav, and Ankita Sarkar

Abstract

The use of chemicals in agriculture to achieve the highest yield was trending in farming practices, which led to the depletion and shifting of microbial community over the years. In sustainable agriculture, the use of organic products was the innovative approach along with the incorporation of microbial products to enhance the growth and productivity of the crop with minimizing the various biotic and abiotic stresses. Instead of adding the microbial population to the soil, conservation of microbial population or microbiome by adopting the various

M. M. Rashid Department of Plant Pathology, Bihar Agricultural University, Sabour, Bhagalpur, Bihar, India Department of Mycology & Plant Pathology, Institute of Agricultural Sciences, Banaras Hindu University, Varanasi, Uttar Pradesh, India B. Teli · S. Belbase · A. Sarkar (*) Department of Mycology & Plant Pathology, Institute of Agricultural Sciences, Banaras Hindu University, Varanasi, Uttar Pradesh, India G. Kumar Krishi Vigyan Kendra, Rajendra Prasad Central Agriculture University, Pusa, Samastipur, Bihar, India P. Dobhal Department of Plant Pathology, College of Agriculture, G.B. Pant University of Agriculture and Technology, Pantnagar, Uttarakhand, India D. L. Yadav Plant Pathology, Agricultural Research Station, Agriculture University, Kota, Rajasthan, India J. S. Patel Department of Botany, Institute of Science, Banaras Hindu University, Jamuhar, Bihar, India S. K. Yadav Narayan Institute of Agricultural Sciences, Gopal Narayan Singh University, Jamuhar, Bihar, India # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2022 U. B. Singh et al. (eds.), Re-visiting the Rhizosphere Eco-system for Agricultural Sustainability, Rhizosphere Biology, https://doi.org/10.1007/978-981-19-4101-6_3

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strategies was the most prominent approach in sustainable agriculture, which enhanced the income of farmers as well as improved the growth and development of the crop. This chapter highlights the importance of microbial community, keeping the rhizosphere parameters in view and utilizing their activity to develop enrichment strategies for the growth and development of plant system.

3.1

Introduction

Agriculture and the environment have a ‘hand in hand’ relationship that is justified through the footprints of agriculture on the environment and vice versa. Both entities have a very significant role in influencing the functional aspects of each other. Agriculture and related practices have huge contributions to climate change, water degradation, land degradation, and many more processes. Simultaneously, the environment also has a huge part to play in agricultural systems (Rockström et al. 2017). The conflict between the agricultural community to increase the production and/or productivity to meet the demands of the growing population and environmentalists to save or exert the least negative impacts on the environment gave rise to the term ‘sustainable agriculture’ (Gold 1999). Thus, for achieving sustainability in agriculture, we have to incorporate alternate input options in the package of practices instead of the chemical alternatives such as synthetic fertilizers, pesticides and insecticides. One such alternative is the utilization of beneficial microbes that can provide nutrients to crop plants and protect them against various abiotic and biotic stresses. Plant microbiome is known to bring different changes in the surrounding and the host plant itself according to the varying set of environmental conditions. These changes support the survival of plant and hence are believed to help achieve the goal of sustainable agriculture. Plant microbiome is defined as the total of all microbes that are associated with a host plant. It is further divided into two groups, namely phyllosphere microbiome and rhizospheric microbiome, depending on the part of the plant they inhabit (Berendsen et al. 2012; Turner et al. 2013; Schlaeppi and Bulgarelli 2015; Rodriguez et al. 2019). Among the two, roots are the primary microhabitat for all the plant–microbe interactions and the microbe–microbe interactions and also the site for inhabitation of a more diverse range of microbes than phyllosphere (Jones et al. 2009; Singh et al. 2019). Besides, the rhizospheric microbiome or rhizobiome has been proven to embellish the growth and yield of crops that are regulated by certain environmental factors like the plant genotype, climate, soil, and human activities (Igiehon and Babalola 2018). Rhizobiome of a plant is present in three root sites, namely: endorhizosphere, rhizoplane, and rhizosphere. The area inside the root within cells and between the cells is known as endorhizosphere, the surface of root is known as rhizoplane and the region of soil surrounding the roots of plant is known as rhizosphere (Reinhold-Hurek et al. 2015). Rhizobiome is also considered as a plant’s second genome (Berendsen et al. 2012). The microbes constituting the rhizobiome carry out different ecological processes and biogeochemical cycles (Philippot et al. 2009). The rhizobiome is the largest prevalent ecosystem on this planet owing to the innumerable microbes, countless interactions, and immense energy flux (Barriuso

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et al. 2008). Hence, it is very necessary to have comprehensive knowledge about the structure and function of rhizobiome. A detailed understanding even about the general structure and function of rhizobiome can be utilized in improving crop health and yield (Vukanti 2020). There is a need for the development of novel techniques that can help in the conservation of this rhizobiome of crop plants and thereby aid in achieving the goal of sustainable agriculture. Soil is the medium that provides the base as well as the materials essential for plant growth and survival. The rhizobiome is also a part of the soil and its composition has an intimate relationship with the plant’s health (Yang et al. 2019). With advent of the Green Revolution, there has been overuse of synthetic fertilizers, pesticides, monocropping, and other input-intensive practices that have caused a serious disbalance in the ecological systems. Since rhizobiome is a fundamental part of the ecological system, their diversity and population also got affected (Du et al. 2020). The rhizobiome is involved in many of the processes in the soil environment, which include conversion of energy, cycling of nutrients, and health of plants (Zhang et al. 2019). Some of the microbes of the rhizobiome also possess the capacity to degrade the contaminants and pollutants from the soil and thus fulfil the purpose of bioremediation (Dubey et al. 2020). Many microbes of rhizobiome by virtue of their metabolic processes supply materials to the plants and also reduce the risk of infection by phytopathogenic microbes (Leghari et al. 2016; Lu et al. 2019; Zilli et al. 2020; Peng et al. 2020). Additionally, the rhizobiome also has microbes that are deleterious to plant health and development, but their population and action are kept in check by the beneficial microbes of the community. The composition and stability of rhizobiome have an intimate relation with plant health and development (Xia et al. 2016). It is proved time and again that the proportions of beneficial and harmful microbes can be modified to obtain a steady state of rhizobiome so as to embellish the health of a plant and strengthen its resistance to different stresses, which in turn will increase the production and productivity sustainably (Du et al. 2020). In this chapter, we present the possible path for achieving the goal of sustainable agriculture through the conservation of rhizobiome.

3.2

Importance of Rhizobiome in Agriculture

The importance of rhizobiome in agriculture can be emphasized from the fact that the crop plants and the rhizospheric microbes have an intimate relationship that is beneficial, pathogenic, or non-effectual, based on the plants and microbes involved. The relationship between plant and rhizobiome decides the survivability of the host plant (Olanrewaju et al. 2019). The communication between them is bi-directional since the plant regulates the composition and dynamics of its rhizobiome through root exudates as well. Our attempts to enhance plant productivity by whatever means have put soil under extreme pressure. The microbes inhabiting the soil are an indispensable part of the soil system and in most cases aid in the growth and development of plants. Exploiting these beneficial effects of microbes on a plant in achieving the target of higher yields and sustainable agriculture can come in handy

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while simultaneously relieving pressure from the soil. Talking about the beneficial effects, the rhizobiome can increase the growth of a plant by enhancing its resistance to phytopathogens, water retention capacity, and nutrient uptake (Evelin et al. 2009; Berendsen et al. 2018). The beneficial relationship between plant and rhizobiome has been studied comprehensively for biological control, promotion of plant growth, and activities in biogeochemical cycles. All these three play an essential role in maintaining the good health of a plant. Some of the microbes in rhizobiome have been proven to be highly useful for plants especially during unfavourable and harsh growing conditions (Meena et al. 2017). Thus, there is an increasing importance of rhizobiome conservation in agriculture as a potential method for achieving sustainability along with higher productions (Igiehon and Babalola 2018). The importance of rhizobiome in agriculture can be demonstrated through their two sets of activities. First set of activities consists of functions and processes that change the dynamics of a plant’s surroundings, and edaphic and climatic conditions, bringing indirect effects, and the second set of activities consists of functions and processes carried out by the microbes of rhizobiome that have a direct effect on plant systems. Many microbes present in the rhizosphere are capable of degrading soil contaminants and are often used as bioremediators (Dubey et al. 2020). Different metabolic activities of different microbes of rhizobiome increase the availability of nutrients such as nitrogen, phosphorous, and potassium. These two actions of rhizobiome microbes aid in increasing the soil fertility and productivity and ultimately the growth and health of a plant (Lu et al. 2019). One of the prime examples of rhizospheric microbe, which increases the availability of nutrients in the soil, is Rhizobium. They fix the inert nitrogen present in the atmosphere to the soil and convert them to ionic forms that are readily available to the plants for uptake. This is achieved by the microbe through a series of chemical processes that subsequently provide nitrogen to plants in an immobilized form (Leghari et al. 2016). Its importance in the sustainable approach of making nitrogen available to crop plants is very well established (Zilli et al. 2020). Many microbes also convert unavailable phosphorus to available forms through the actions of organic acids and enzymes. In addition to this, the beneficial microbes of rhizobiome also eliminate and reduce the population of phytopathogenic microbes (Wang et al. 2015; Lu et al. 2019; Peng et al. 2020). This is achieved through their antagonistic actions against the phytopathogenic microbes, which comprise antibiosis, parasitism, and competition for space and resources (Cabot et al. 2018; El-Sharkawy et al. 2018). Direct effects on crop plants by the beneficial microbes of rhizobiome are through the production of phytohormones, enzymes, siderophores, and induction of defence responses in plants. Beneficial microbes like Trichoderma, which is a part of many plant’s rhizobiome, is known to produce auxin, gibberellins, and 1-aminocyclopropane-1-carboxylate (ACC) deaminase that embellish the growth of a plant (Jaroszuk-Ściseł et al. 2019). Trichoderma spp. have also been known to induce production of peroxidases, polyphenol oxidases, chitinases, and β-1,3-glucanases in crop plants, which help in defending them against the phytopathogens (Baiyee et al. 2019). Some of the microbes also induce the expression of pathogenesis-related genes in crop plants, which also helps in the same (Sun

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et al. 2018). The endophytic constituents of rhizobiome form a symbiotic association with the host plant and directly provide nutrients and water to plants (Spagnoletti et al. 2017; Stürmer et al. 2018). The beneficial bacterial population of the rhizobiome also acts as plant-growth promoters through many actions that have direct effects on plants (Jogaiah et al. 2016; Patil et al. 2016; Misra et al. 2017). Many of the plant-growth-promoting rhizobacteria (PGPR) also increase the content of alkaloids in plants, which helps in warding off the ill-effects of abiotic stresses and simultaneously increasing the nutritional status (Rajasekar and Elango 2011; Ghorbanpour 2013). Talking on the front of the phytopathogenic component of rhizobiome, regulation and manipulation of their presence and population can bring undoubted improvement in plant health. Since a myriad of microbes form the rhizobiome of a plant and have a significant effect on the plants as well as the soil, a deep understanding and deciphering of the underlying mechanism would certainly help in improving the production in agriculture along with achieving sustainability. This would open many avenues for ensuring global food security as well (Xie et al. 2019). Framing of crop plant breeding programmes for breeding a genotype that can recruit or change the dynamics of its rhizobiome according to the available environmental conditions is a booming prospect (Wei and Jousset 2017). This would help in achieving an environmental adapting genotype of crop plants through recruitment of rhizospheric microbes. Soil amendments and seed treatment with beneficial microbes is also another approach that can lead to a changed structure of rhizobiome of a crop plant and that has been proven to be effective in increasing the yield and adaptation to several abiotic and biotic stresses. These augmentation techniques bring beneficial changes in plant– microbe interactions and lead to the establishment of an associative and symbiotic relationship. The rhizospheric microbes that act as bioremediators will certainly help in the alleviation of degraded agricultural lands. Additionally, many unproductive and unfertile lands can be turned into productive and fertile agricultural fields by the application of beneficial microbes present in the plant’s rhizobiome. They can either work in association with their host plant (generally) or alone (exceptions) in making the soil fertile and productive. The rhizospheric microbes with biological control activities can be utilized as a potential tool for the management of various phytopathogenic diseases in crop plants and to reduce the dependence of the farming community on synthetic pesticides.

3.3

Understanding the Rhizosphere Ecology, Biology, and Microzone

Total microorganisms present in a community has been considered as microbiome (del Carmen Orozco-Mosqueda et al. 2018). Similarly, all the microorganisms present in the rhizosphere constitute the rhizosphere microbiome. The complex community present in the rhizosphere can be treated as plant’s secondary genome, which contains microorganisms as well as other genetic elements affecting plant health (Berendsen et al. 2012). The functioning of rhizobiome for plant growth

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promotion and defence is not well explored due to the unavailability of suitable tools and techniques. Several efforts have been made to understand the role of rhizobiome, such as the use of the latest sequencing techniques for the metagenomics of the rhizospheric soil (Turner et al. 2013; Schlaeppi and Bulgarelli 2015). Sequencing techniques along with metabolomics, metagenomics, proteomics, metatranscriptomics, and transcriptomics can be helpful to understand the microbial diversity of the rhizosphere. Furthermore, these techniques can also unravel the relationship between plants and microbes present in the rhizosphere for plant health and plant protection. Microorganisms present in the rhizobiome can be divided into two groups: either beneficial or non-beneficial. Human pathogenic bacteria can make an inter-kingdom jump due to the presence of the microsites on plants (Holden et al. 2009). The genotype of the plant, species of the plant, and the constituent of the soil determine the recruitment of specific microbes in the rhizosphere (Bakker et al. 2012). A few reports (Mendes et al. 2013; Lakshmanan et al. 2014) suggested the role of malic acid in the stimulation of Bacillus subtilis in the rhizosphere. Rhizobiome can influence the plants in several ways as there is the existence of both beneficial and non-beneficial or pathogenic microorganisms (Liu et al. 2015). Bever et al. (2012) suggested the existence of both positive and negative associations between plant and rhizospheric microorganisms.

3.4

Assessing the Rhizobiome in Different Ecosystems

Several microorganisms are associated with the rhizosphere of the plant, collectively known as rhizobiome. These microorganisms are involved in nutrient acquisition for plants or acquiring nutrients from the plant, impacting the plant health positively as well as negatively. Several factors such as plant genotype, species of plant, and rhizosphere environment are affecting the recruitment of these microbes. Several reports (Gottel et al. 2011; Shakya et al. 2013; Cregger et al. 2018) suggested the use of next-generation sequencing for the study of rhizobiome. The presence of fungi and bacteria in the rhizosphere is influenced by the host species (Bonito et al. 2014). The genotype of the plant more prominently govern the recruitment of the microbes (Bálint et al. 2013; Cregger et al. 2018) in the above-ground part of the plant tissues, including leaves and stem. Soil is the major factor governing the composition of Populus rhizospheric microorganisms such as fungus and bacteria (Bonito et al. 2014; Cregger et al. 2018). Major diversity of cellulolytic and antagonistic organisms including Trichoderma viride and Humicola grisea was found around the plant rhizosphere. Several findings (Kaushal et al. 2018; Ahmed 2018) reported the role of Trichoderma species in the biological control in the natural agricultural systems. The presence of Trichoderma species in the rhizospheric soil reduces the soil-borne pathogens and strengthens the plant against the pathogens present in the foliar region (Oancea et al. 2017). The reports are suggesting the role of these beneficial microorganisms in the improvement of soil texture, which ultimately improves soil

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aeration as well as strengthens the plant resistance against biotic and abiotic stresses. Fungi have the ability to mobilize the nutrient as well as to help in the nutrient uptake due to the production of the enormous hyphal network around the plant roots (GaraySerrano et al. 2018). Several microbes found in the region of Babadag plateau in Rendzic Leptosols were reported having the ability to help in soil formation by nutrient recycling, decomposition of the cellulose as well as humus formation. The secondary metabolites secreted by the microbes in the rhizosphere help in the aggregation of soil and make the soil environment favourable for the plant growth. Few of the reports suggested the role of beneficial microbes for selective suppression of the pathogenic microbes in the rhizospheric soil (Alabouvette and Steinberg 2006). Different modes of interactions are present in the rhizosphere with microbes including symbiosis, predation, and competition. The role of edaphic microorganisms was also suggested (Wieder et al. 2013) for carbon sequestration and controlled emission of CO2. Microbial secondary metabolites contain antimicrobial actions as well as several enzymes that can be used commercially for biotechnological purposes (Marco et al. 2003; Mapari et al. 2005). Beneficial microbes can be used for the biocontrol purpose, which could ultimately reduce the use of hazardous biochemical (Hanson and Howell 2004; Namdeo 2007; Matei and Metei 2008). We can talk about the study on seagrass, which are marine flowering plants found in the intertidal and shallow subtidal zones, to know about the microbial structure of this ecosystem. These plants are mainly responsible for the coastal ecosystems by serving as a food source, space for the animals, stabilizing sediments, and nutrient recycling. The root zone of the plant contains both the beneficial and non-beneficial microbes. Different species of this plant contain different kinds of microbial diversity in their respective rhizospheres and it was suggested that the rhizobiome includes mainly bacteria related to the sulphur cycle and is affected mainly by the plant metabolism. The rhizospheric ecosystem of solanaceous plants is one of the important ecosystems for the agricultural system. Two plants including tomato (Solanum lycopersicum) and chilli pepper (Capsicum annuum) are of major economic importance. These plants are known to exhibit different microbes in their rhizosphere, involved in governing the host plant health and its productivity. The assembly of rhizobiome has been proposed to take place in two steps. First, the rhizosphere is colonized by a subgroup of the soil microbial community inhabiting the bulk soil, and then the rhizoplane and the endosphere is colonized by the subgroup of the earlier colonized rhizospheric microbial community. All the microbes that get associated with the plant form a core microbial community of the rhizobiome. This core microbial community has both fungal and bacterial species that are common to many species of plant (Sasse et al. 2018; Olanrewaju et al. 2019; Ávila et al. 2019). The accumulation of microbes from the bulk soil community is due to the richness of nutrients in the rhizospheric region by the accumulation of exudates secreted by plants, which consist of sugars and amino acids. These sugars and amino acids serve as the source of carbon and nitrogen for the microbes due to which they get attracted to the rhizosphere. According to the ‘cry for help’ hypothesis, plants also secrete certain unique metabolites or some general metabolites in

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large concentration to recruit the soil microbes that help them in the alleviation of stress faced by plants in a particular time and place (Rolfe et al. 2019). The microbes of rhizobiome which settle on the root surface of the plant or the rhizoplane generally mobilize the inorganic nutrients from their immobilized forms and also fix those present in the atmospheric region which indirectly helps in plant growth promotion (Lopez et al. 2011). The microbes of the rhizobiome that enter the intercellular space of root tissues in a plant without harming the plant are known as endophytes. They induce resistance to phytopathogens by modulating the defence genes of plants (Passari et al. 2016; Sasse et al. 2018). In the earlier microbiome studies pertaining to agriculture, the main focus was to find the influence of different packages of practices on the soil microbial complex and generally excluded the factors related to the host genotype and those related to the interaction of agricultural practices and host genotype (Gomez-Montano et al. 2013; Hartmann et al. 2015; van der Heijden and Hartmann 2016; Poudel et al. 2019). In advance studies, the effects of host genotypes were also included and it was observed that there is a significant variation in the structure and composition of rhizospheric microbial complex depending on the genetic background of a plant in many crops like maize, rice and Arabidopsis (Bulgarelli et al. 2012; Lundberg et al. 2012; Peiffer et al. 2013; Edwards et al. 2015; Lebeis et al. 2015; Mendes et al. 2018). These variations in the rhizospheric microbial complex can be explained physiologically due to the varying nature of root exudates and rhizodeposits of a plant species, which is regulated by the genetic constituents (Nasholm et al. 2000; Uren 2007; Reeve et al. 2008). Through this varying nature of root exudates and rhizodeposits, plants provide specific cues that recruit selected microbes from the bulk soil microbial community (Zhalnina et al. 2018; Beattie 2018). The root exudates and rhizodeposits also contain certain molecules that deter away the pathogenic or non-beneficial microbes (Hassan and Mathesius 2012). The findings from these advanced studies suggested that there is a host-specific microbiome filter that functions actively in the selection and recruitment of specific microbes in its rhizobiome. The rhizobiome, thus, varies from plant to plant and genotypes to genotypes (Lundberg et al. 2012; Edwards et al. 2015; Panke-Buisse et al. 2015; Fonseca-García et al. 2016; Wang et al. 2017; Cregger et al. 2018).

3.5

Effect of External Parameters on the Rhizobiome

Rhizobiome determines the overall wellbeing and productivity of the plants (Lakshmanan et al. 2014). It prompts various functioning expressions in plants like productivity, robustness, and fecundity. Inspecting plant rhizobiome assists in knowledge of the interaction between plant and rhizobiome along with genetic and functioning of the host and key metabolic and physiological facets of rhizobiome complex (Rout and Southworth 2013). The interconnection between the plant and rhizobiome needs a bridge that connects them like root exudates and soil parameters. This assists plants in interacting with the rhizobiome affecting the plants significantly (Bais et al. 2006). The rhizobiome reacts to the root exudates acting as a

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signalling molecule. Exudates comprise of various components like mannose, arabinose, glucose, amino acids, fatty acid, nucleotides, auxin, enzymes, alkaloids, flavonoids, and vitamins (Gunina and Kuzyakov 2015; Hayat et al. 2017). Besides these compounds, other key carbon compounds produced from plant roots are carbon specified by photosynthesis (Bamji and Corbitt 2017). The microbes release consequential compounds modifying the mechanism of plant and signals aid in acquiring nutrition (Brazelton et al. 2008; Kim et al. 2011). The symbiotic association between host plant and the microbes of the rhizobiome has been studied; their interaction, progression, and ecology of symbioses have not been studied extensively. The rhizobiome plays elementary role in nutrition of the plants. The root-associated fauna plays important role in advancement of plants and the associated biosphere (Fitzpatrick et al. 2018).

3.5.1

Overview of Rhizobiome Structure in Agricultural Fields

The investigation of the rhizobiome will magnify the understanding of the growth and development of the plants (Mendes et al. 2013). For instance, methanogens are usually existing in the geographical areas where paddy is cultivated. The knowledge of this fact might enhance the possibilities involved in the methane cycle. Other than this, it also gives knowledge about other correlated microbes of paddy along with other flora present (Edwards et al. 2015). It was noticed that the diversity of the microbes in the paddy field has a remarkable impact on the field. The rhizospheric studies reveal that rhizobiome is immensely affected by the site of cultivation. It is evident that with different plant attributes the microbes in the vicinity of the root system also differ, i.e. attributes differ among endosphere and rhizosphere systems. The rhizospheric variegation was found emphatically linked to the productive capacity of the host plant and obstructively related to the stretch of the rootstock whereas the diversification of the endospheric complex was found related to the density of root hair (Fitzpatrick et al. 2018). The kind of soil along with the environment affects the structure of the rhizobiome. Other than this, the genotype of the host and root exudates impact the rhizospheric complex (Haney et al. 2015). The microflora of the rhizobiome harmonize with the plants in the ecosystem, so they might have coexisted in agreement to the requirements of one another for being compatible in the ecological system (Philippot et al. 2013). By modifying the constituents of the exudates of the plant, roots stimulating the liberation of an increased quantity of beneficial exudates through re-programming of plant microbes can enrich the rhizobiome (Přikryl et al. 1985; Bulgarelli et al. 2012). Hence, the antimicrobial and secondary metabolites play important role in establishment and competition for space within the rhizobiome. To achieve better communication among rhizobiome, plant and environmental conditions, competition for supremacy and establishment is important. Paddy is grown in submerged soil. The oxic areas are developed in the rhizosphere. It is adjoined by anoxic soil due to the release of O2 by the means of aerenchymatous cells present in the root system of rice plants (Yuan et al. 2016; Zhao et al. 2019). The oxic and anoxic complexes thus

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developed influence the microbial community (Revsbech et al. 1999; Li and Wang 2013). The studies on Brachypodium and maize revealed that the type of microbial community differs with the type of root system (Kawasaki et al. 2016; Yu et al. 2018). Even microbial complex may differ with various tissue of the plant.

3.5.2

Factors Related to the Development of Rhizobiome

Soil, surrounding environment and host plant influence the formation of the rhizobiome; for example, the microbes including fungi and bacteria differ with the type of soil and root system in Populus. The microorganisms of a particular taxon are not linked to the genotype of Populus. The studies have revealed that microbes are from the order Burkholderiales, Rhizobiales, Chitinophagales, and Cytophagales (Bonito et al. 2019). The experimental studies on the rhizobiome of Populus dissociate the genotype of the plant under the impact of structure and properties of soil affecting the microbial communities (Bonito et al. 2019). It was also evident that the texture of the soil, geographical area and extent of phosphorus are positively related to the microbial communities. This reveals that the taxon of the microbes is not the same all around the landscape and the rhizobiome is affected by soil and ecological conditions. It became obvious from different studies that variability between rhizospheric and endospheric communities of Populus deltoides was because of variations in topographic, climatic, and habitat conditions. Such results were also found in Pinus, Arabidopsis, and Agave (Lundberg et al. 2012; Talbot et al. 2014; Fonseca-García et al. 2016). It was also noticed that the rhizomicrobiome of a plant is affected by the genotype and species of the host (Bonito et al. 2014). The above- and below-ground parts have different impacts on the microbiome (Bálint et al. 2013; Cregger et al. 2018).

3.5.2.1 Effect of Vermicompost on Rhizobiome The organic matter available in the soil comprises of microbes. The microorganisms present in the soil react to functions of the surrounding environment and soil like nutrient cycle, putrefaction, and suppressing of pathogens (Doran and Zeiss 2000). The amount of organic content checks the activity of the microbes, including more amounts of nitrogenous compounds in soil. Applying vermicompost enhances biomass and diversification of the microbes in the soil. Vermicompost along with earthworm casts provides a magnificent channel to harbour bacteria for nitrogen fixation in the soil. There was a significant increase in Gram-negative bacteria following application of increased dosage of vermicompost (Lazcano and Dominguez 2011). A generous amount of vermicompost enhances the community of microorganisms like Bacillus stearothermophilus, Azotobacter chroococcum, and Pseudomonas putida. The microbial activity activated by vermicompost intercepts leaching of the nitrogen.

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3.5.2.2 Effect of Biochar on Rhizobiome Soil biome is essential for proper processing of ecosystem functions. Biochar addition affects the biome of the rhizosphere by enhancing the structure and functions of the microbial population (Steiner et al. 2008; Hammes and Schmidt 2009; Hongyan 2010; Liang et al. 2010; Chintala et al. 2014). An increased amount of colonies of Trichoderma and Bacillus was observed upon application of biochar (Graber 2009). The application of biochar makes the soil pH appropriate for the microbial communities (Wuddivira et al. 2009). It provides a satisfactory domain for colonization, reproduction, and growth ability for rhizobiome (Thies and Rillig 2009). 3.5.2.3 Effect of Chemical Pesticides on Rhizobiome The application of pesticides might change diversification of the microbes in soil resulting in deterioration of soil fertility (Lo 2010). The application of pesticides contaminates the soil making it noxious to rhizobiome (Aktar et al. 2009). Arbuscular mycorrhiza boosts doorway for water and minerals for the plant, enhancing its drought sufferance etc. Application of herbicides, however, turns down the establishment of arbuscular mycorrhiza (Druille et al. 2013). The soil biome is damaged by the application of herbicides (Nicolas et al. 2016). The pertinacious ability of herbicides in soil is hazardous to the biome of rhizosphere, which is advantageous to crop productivity (Thiour-Mauprivez et al. 2019). These noxious chemicals contaminate the soil and water resources (Noshadi and Homaee 2018). A reduction in community of microbes was observed after applying herbicide (Silambarasan et al. 2017) (Table 3.1).

3.6

Conservation Strategies for Enriching the Soil with Useful Rhizobiome

Rhizobiome that has been reported to increase plant growth, development, and yield is influenced by various factors such as climate change, plant cultivar, anthropogenic activities, and soil types. Even the age of the plant also has an influence on the rhizospheric microbiome (Chaparro et al. 2014). In anthropogenic activity, we use chemical fertilizers for the fulfilment of nitrogen, which is directly linked with environmental degradation greatly affecting the plant rhizobiome. We can replace/ reduce the chemical nitrogen-based fertilizers by using the nitrogen-fixing freeliving and endophytic rhizobacteria that can help secure the rhizospheric microbial communities. Different species of Rhizobium, Bacillus, and Azospirillum have been reported to enhance the biomass of plants in case of both above and below ground, which ultimately results in a positive impact on the crop for sustainable agricultural production (Igiehon and Babalola 2018). The rhizobiome of a plant is less diverse than that of the surrounding soil and the microbial diversity mainly leads a narrow bacterial lineage. A study of rhizobiome associated with dicots and monocots, viz. Arabidopsis (Bulgarelli et al. 2012; Lundberg et al. 2012), sugarcane (Yeoh et al. 2016), maize (Peiffer et al. 2013),

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Table 3.1 Chemical effect on different rhizospheric microorganism S/ N 1

Chemical type Herbicide

Name of chemical input Glyphosate

2

Herbicide

Glyphosate

3

Herbicide

Glyphosate

4

Fungicide

Mancozeb

5

Herbicide

6

Herbicide

Atrazine, pendimethalin Pendimethalin

7

Herbicide

Triclopyr

8

Insecticide

Methamidophos

9

Herbicides

Glyphosate

10

Herbicide

2,4-D

11

Fungicide

Butachlor

12

Insecticide

Fenamiphos

Effects Toxic to soil fungus Aspergillus nidulans Reduces the spore viability of arbuscular mycorrhizal fungi (AMF) Increased frequency of the soil-borne fungus Fusarium solani Total fungi, actinomycetes and Pseudomonas bacteria were significantly reduced Lower microbial population Significant reduction of soil microbe population Inhibits soil bacteria that transform ammonia into nitrite Significantly decreases microbial biomass by 41–83% Reduces growth and activity of freeliving nitrogen-fixing bacteria in soil Inhibits the transformation of ammonia into nitrates by soil bacteria Reduced population of Azospirillum and aerobic nitrogen fixers in non-flooded soil Detrimental to nitrification bacteria

References Nicolas et al. (2016) Druille et al. (2013) Sanogo et al. (2000) Magarey and Bull (2003) Silambarasan et al. (2017) Nalini et al. (2013) Pell et al. (1998) Wang et al. (2006) Santos and Flores (1995) Martens and Bremner (1993) Lo (2010)

Lo (2010)

rice (Edwards et al. 2015), oak (Uroz et al. 2010), lettuce (Schreiter et al. 2014), and barley (Bulgarelli et al. 2015), reveals the presence of dominant phyla (especially proteobacteria and actinobacteria) and certain bacterial lineages found consistently more in the rhizobiome. The soil type is a key factor in determining the rhizobiome because of the plant recruiting the rhizobiome first and foremost from the soils they reside (Bulgarelli et al. 2013; Sarma et al. 2015). The molecular survey of cultureindependent rhizobiome reveals the influence of soil type on microbial community being stronger than that of the host plant. However, such types of research have mainly been performed on model crops (Yeoh et al. 2017). Further, the secondary factor other than the soil type is plant host phylogeny that influences rhizobiome, but the effect is particularly less than soil type (Bulgarelli et al. 2012; Lundberg et al. 2012). Similarly, the comparison of rhizobiome in maize, wheat and sorghum (monocots) (Bouffaud et al. 2014) and Arabidopsis and Cardamine hirsuta (eudicots) (Schlaeppi et al. 2014) reveals the major variation in rhizospheric microbial communities of the two outlying plant species. Hence, it is clear that the host phylogeny of plants also has greater influences on rhizobiome composition. Overall, the research exhibits the establishment of core rhizobiome before the evolution of

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various plant lineages and these microbial communities evolved themselves with their host plants, and the functions of rhizobiome are also found conserved. In another study, the independent root and endospheric metagenome showed similar functionality such as bacterial motility, protein secretion system, iron acquisition, and nitrogen metabolism in rice, wheat, and cucumber (Sessitsch et al. 2012; OfekLalzar et al. 2014). In the findings of these studies, we get a list of bacterial lineages for further research in their plant–microbe interactions accompanying rhizobiome recruitment, function, persistence, turnover etc., and the knowledge about these things might be helpful to enhance crop production (Yeoh et al. 2017). Hence, the knowledge that the interaction of plant-phylogeny-related rhizobiome and soil type influenced rhizobiome becomes more significant to conserve rhizobiome, so that the benefits in crop productivity can be enhanced (Sarma et al. 2015). The conservation practices for a particular plant and related rhizobiome would be helpful to enhance plant health and production. Among them, certain practices are linked with plant processes that influence their growth. Further, the plants can be manipulated to change the pH of rhizosphere, release compounds to improve nutrient availability and enhance the growth of rhizobiome by protecting them from various abiotic and biotic stresses. Similarly, the rhizobacteria present in rhizobiome that are beneficial in plant growth can be engineered to regulate the synthesis of plant hormones that are helpful in plant growth and production of various antibiotics and enzymes to cope up with soil-borne diseases. Rhizobiome conservation is also assisted by the plant because plant can modify the beneficial microbial communities to enhance the proliferation of certain antibiotic-producing strains that make soil suppressive to soil-borne diseases. The fitness and richness of rhizobiome can be improved by soil reclamation that permits the selection of microbial consortium against the various soil-borne pathogens. The amendment in the plant through genetic engineering also plays important role in influencing the rhizobiome, and the best example is quorum quenching mechanism that inhibits the virulence in Pectobacterium.

3.6.1

Conservation Through Manipulation of Rhizospheric pH

The rhizospheric pH plays an important role in the conservation/richness of the rhizobiome. The pH of rhizospheric soil is greatly influenced by the exudates secreted from plant roots. The pH is a negative logarithm of H+ concentration; that means a higher concentration of H+ in the rhizosphere lowers the pH and vice versa. The proton efflux from the plant roots is governed by H+-ATPase protein family that utilizes energy from adenosine triphosphate (ATP) to pump H+ via plasma membrane against the electrochemical gradient. The H+ efflux also contributes to the nutrient acquisition by solubilizing certain elements in the rhizosphere due to a lowering in pH (Hinsinger et al. 2003). Lowering pH creates local acidifications that lead to the enhanced availability of phosphorus and iron, which are generally fixed in the insoluble complex form in the soil. In dicots and monocots other than Gramineae family, the iron uptake involves the secretion of iron-chelating compounds that

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reduce the Fe3+ to Fe2+ before the uptake. There are various microbes present in rhizosphere that enhance the reduction process and make iron available in a soluble form that can be taken by plants. In contrast, grasses release the phytosiderophores for the same process and make iron available to the root surface for absorption (Neumann and Römheld 2007). Similarly, the release of organic acids, viz. malate and citrate, along with certain enzymes like phosphatases and phytases promote the growth of certain microbes to access hardly soluble inorganic and organic phosphorus (Dinkelaker et al. 1995; Vance et al. 2003; Ryan et al. 2009). These organic compounds’ efflux is also responsible to protect certain crops and microbes from Al3+ toxicity by chelating Al3+ ions in acidic soil and thus preventing the damage at root apical meristem (Ryan et al. 2009). Hence, the release of elements and compounds from plant roots helps in plant growth by providing nutrients. The organic acids secreted from roots also help in rhizodeposition. These root exudates, thus enhance nutrient acquisition, tolerance to mineral stresses and stimulate the growth of beneficial microbes by conserving the rhizobiome.

3.6.2

In Situ Conservation of Rhizobiome

In situ conservation of rhizobiome is the conservation of microbial diversity present in rhizobiome protected in their natural environment, i.e. in various geographical locations that are defined as hotspots. The deep-water rice, copper mine wasteland, Prairie plants and agronomic crops, pea cultivar in field conditions, grass ecosystem and Polar regions are the examples. Conservation, in natural areas, of populations of high-valued microbes is the basic condition for conservation of the rhizobiome. The strategies for conservation of certain endophytic species of plant genus Zea were explored and it was found that the domestication of its wild ancestor (teosinte) to current maize (corn) evolved from Mexico to Canada. The study revealed the presence of core microbiota conserved in Zea seeds during the evolution (Johnston-Monje and Raizada 2011). In another molecular study in Silene paradoxa, the bacterial communities of seeds showed the transfer of endophytic bacterial community into the next generation of the plant. Hence, this study sets an example that specific plants from a particular location might be helpful in in situ conservation of endophytic microbial community (Mocali et al. 2017). In recent past, in situ conservation provides the opportunity to reveal greater diversity of microbes in the environment, where the total and culturable rhizobiome of wheat plant is conserved in microwell chambers (MWCs) (Acuña et al. 2020). Therefore, in situ conservation can be an appropriate means for the conservation of rhizobiome.

3.6.3

Ex Situ Conservation of Rhizobiome

Ex situ conservation of microbial diversity means the conservation of microbes and their factors outside their natural environment. The factors mean the gene banks, man-made wild field banks of microbes with plants, artificial propagation of plants

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with their rhizobiome, botanical gardens and microbial culture collections. Ex situ conservation is involved in the conservation of genetic resources of microbial communities, and protects them from extinction. The establishment of microbial culture collection was started in the late nineteenth century and microbes were isolated on various growth media in pure culture and maintained in the laboratory with the mandate distribution of microbial strains for the purpose of research (Smith 2003). The idea for establishing the culture collections is valuable due to the availability of microbes for basic research and agricultural purposes. The repository or culture bank is useful in exploring the evolutionary and metabolic patterns of important microbes that play a major role in industry, agriculture, and health divisions (Sharma et al. 2017).

3.7

Impact of Rhizobiome on Soil Enrichment Along with Plant Growth and Development

The microbial diversity present in the rhizosphere of a plant is considered as rhizobiome, which normally helps in better growth of the host plant. The rhizobiome present in the rhizospheric region of plants can be influenced by various signalling mechanisms between the plants and microbes as per the requirement. The rhizospheric microbial community enhances nutrient absorption in plant roots and also increases the availability of nutrients from distant sources directly and indirectly (Vessey 2003). Various rhizospheric microbes oxidize manganese in the rhizosphere to reduce the toxicity of manganese in the plant grown in less oxygen conditions in saturated soil. However, few of them also improve manganese availability in aerated soil with high calcium carbonate content (Babalola 2010). Rhizospheric microbes are the major part of PGPRs, which colonize the plant roots and promote plant growth by nutrient absorption and reduction of plant pathogens (Babalola 2010). PGPRs also act as biofertilizers other than by enhancing the indigenous microbial diversity without any negative effects or contamination in soil, unlike conventional agriculture that uses chemical fertilizers (Conway and Pretty 2013; Rascovan et al. 2016). However, each PGPR does not necessarily act as a biofertilizer, e.g. those enhancing plant growth indirectly such as by reducing pathogens and pests cannot be considered biofertilizers as such. However, certain PGPRs act as the agents for both, increasing the plant growth directly as well as indirectly through suppression of phytopathogenic microbial community. For example, Burkholderia cepacia reduces growth of the phytopathogen Fusarium spp. and also enhances maize growth in irondeficient conditions by siderophore production (Bevivino et al. 1998). Certain arbuscular mycorrhizal fungi (AMF) act as pesticides (Babikova et al. 2014). The rhizobiome thus influences the growth of above- and below-ground biomass of plants (Uma et al. 2013). Soils under different environmental conditions vary in their structure, pH, nutrient status, organic matter, and texture. The soil type is also responsible for various activities of rhizobiome present in the plant rhizosphere. The soil pH and availability of organic carbon greatly influence the growth of various plant pathogenic

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nematodes, fungi, bacteria, and beneficial microbes (Rotenberg et al. 2005; Toljander et al. 2008; Dumbrell et al. 2010). The beneficial microbes help the plant by making a symbiotic relationship and support acquisition of nutrients like nitrogen and phosphorus. Other than N and P, iron is an additional nutrient that can be provided to plants by symbiotic relationship with rhizobacteria. However, iron (III) is present in more quantity in soil but plants absorb iron (II) in its reduced form (Salisbury and Ross 1992). Microbes produce siderophores that chelate iron (III) and make it available at the root surface where it is reduced to iron (II) and absorbed immediately (von Wirén et al. 2000). The rhizobiome plays a crucial role in the activation of plant defence against various invading pathogens by stimulating phytohormonal signalling. The microbial communities belonging to bacteria (Burkholderia, Pseudomonas, Bacillus, and Erwinia) and fungi (Trichoderma, Aspergillus, and AMF) are reported to solubilize and mobilize P, Zn, and K in the form that can be easily absorbed by plants (Sudhakar et al. 2000). The P absorption plays an important role in the proper functioning and development of plants from the reservoir of non-soluble form in the soil. The rhizobiome solubilize them and makes them available to the plant (Hameeda et al. 2008; Richardson et al. 2009). Apart from nutrient enrichment and protection from pathogens, the rhizobiome also plays a significant role in the reduction of various abiotic stresses of the plant. Salt, drought, cold, high temperature, and heavy metal toxicity are the most important abiotic stresses that greatly influence plant growth, development, and yield. The study reveals that the activity of various microbes from the rhizobiome helps in stimulating the plant response that is effective against these abiotic stresses. In recent years, the use of microbes is more focused on such types of rhizobiome that assist plant growth and development under stress conditions. This emerging strategy of application of rhizobiome that promotes plant health and copes up with abiotic stresses is gaining global attention. Thus, the rhizobiome of a particular plant not only enriches the soil with nutrients but also protects plants from various abiotic and biotic stresses and promotes better development and yield of the crop.

3.8

Future Aspects

Modernization of agriculture practices poses a severe threat to the microbial community along with some anthropogenic activities including climate change. The role, importance and ecology of the microbiome are emphasized in this chapter along with conservation strategies, highlighting the need to educate the farmers to incorporate such practices for the sake of making their farming sustainable. These microbes can play important roles in biogeochemical cycling by providing the atmospheric N, unavailable phosphorus, facilitating uptake of water and nutrients, making the otherwise unavailable micronutrients available, improving the crop health by reducing the impacts of the biotic and abiotic stresses, and thus enhancing the plant growth and yield of the crop. Ultimately, conservation will help in sustainable farming practices, which is an approach of tremendous importance in enhancing gains

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through better crop health, and achieving food security and conserving the microbiota simultaneously to ensure sustainability in the business of farming.

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Exploring the Rhizosphere Microbiome for Sustainable Agriculture Production Anamika Dubey and Ashwani Kumar

Abstract

Most published research shows that the vast variety of microorganisms present below ground affects the above-ground biodiversity. The rhizosphere is considered the most complicated microbial habitat present on the earth’s surface, often referred to as the secondary genome of the plant. Recent evidence also supported that soil microbial diversity plays a key role in determining terrestrial ecosystems’ evolutionary responses and ecology to ongoing environmental changes. Recent advances in next-generation sequencing have improved the discipline of metagenomics, allowing researchers to get insight into the lives of previously uncultivable microbes. Metagenomics techniques are crucial for elucidating their taxonomic and functional potential and evaluating plant– microbe interactions to improve plant performance in the face of various stressors and to ensure long-term crop production. This chapter highlights key knowledge gaps in rhizosphere biology, summarizes current plant–microbiome engineering researches, and suggests future research directions. Additionally, this chapter emphasizes the need of using metagenomics and bioinformatics methods to get a better understanding of the plant microbiome.

4.1

Introduction

The rhizosphere is the first plant-influenced habitat encountered by the groups of microbes present inside the soil, and therefore it is a narrow zone of contact between the plant roots and soil particles (Dessaux et al. 2016; Kumar and Dubey 2020).

A. Dubey · A. Kumar (*) Metagenomics and Secretomics Research Laboratory, Department of Botany, Dr. Harisingh Gour University (A Central University), Sagar, Madhya Pradesh, India # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2022 U. B. Singh et al. (eds.), Re-visiting the Rhizosphere Eco-system for Agricultural Sustainability, Rhizosphere Biology, https://doi.org/10.1007/978-981-19-4101-6_4

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Majorly, every part of the plant is colonized by varieties of microbes like bacteria, fungi, and viruses, collectively referred to as phytomicrobiome or plant microbiome. Therefore, the rhizosphere microbiome plays a pivotal role in maintaining plant health, providing defense against pests and diseases, facilitating nutrition acquisition, and helping the plant to withstand various stresses (Soni et al. 2017; Kumar and Dubey 2020). The relationship between microorganisms and plants is intimate in so that the microbial population that inhabits and colonizes the rhizosphere, rhizoplane, endosphere, and phyllosphere of plants is regarded as the secondary genome of the plant (Berg et al. 2014). The rhizosphere microbiome contains a huge diversity of microbes that interact with each other in positive and negative ways, just as gut and skin microbial populations impact human health, rhizosphere microbial communities impact plant health. The plant and its microbiota are called as holobionts (Lakshmanan et al. 2014; Dessaux et al. 2016). The positive interactions constitute a symbiotic association between roots and mycorrhizal fungi, epiphytes, and plant growth-promoting rhizobacteria (PGPR). Negative interactions include parasitism by groups of bacteria and fungi and competition created by a variety of herbivores. Evidence suggests that only a small percentage of microbes on the planet (approximately 1%) can be cultured; this illustrates our limited understanding of the structural and functional diversity of the microbial world, as well as the vast emporium of potential medicines and useful industrial products that exist virtually intact in the microbial world (Soni et al. 2017). The root is another essential part of the plant that forms the interface between the plant and the soil environment. Roots release various exudates that interact and cooperate with microorganisms inhabiting soil (Reinhold-Hurek et al. 2015). Important questions need to be answered about these components that contribute to the soil-selective microbial enrichment of the area around the roots or the rhizospheric area (Bais et al. 2006; Doornbos et al. 2012). Previously, carbohydrates were recognized as the general chemical determinants in the rhizosphere, but now amino acids are also considered as chemical determinants present in the rhizosphere (Moe 2013; Soni et al. 2017). Various flavonoids and other secondary metabolites produced by plants were identified as key drivers for the successive formation of host-specific microbial communities in the rhizospheric zone (Weston et al. 2015; López-Ráez et al. 2017). Therefore, the promising avenue for engineering the rhizosphere microbiome is to take the metaorganism into account and try to optimize the whole system instead of optimizing each part separately. The studies conducted by different workers help us to understand the role of these PGPR or plant growth-promoting bacteria (PGPB) isolated from the rhizosphere of the plants for improving health and performance under different types of stress conditions (Ahmad et al. 2012; Kumar et al. 2013, 2015, 2016). Recently, next-generation sequencing (NGS) technologies have made it feasible to study the immense microbial diversity in the rhizosphere in detail. Metagenomics or culture-independent method is a powerful approach for directly analyzing the total genomic content of microbial diversity from the environmental samples (Allan 2014). It is typically based on two approaches: (i) sequence-based approach,

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which involves sequencing of the entire DNA sample, after which the sample is assembled and annotated with a more targeted approach (e.g., 16S rDNA); and (ii) functional approach, which includes the construction of metagenomics libraries in a heterologous host, which are then screened for a particular function. Integration and analysis of the information obtained from both sequence-based and functional metagenomics approaches enable a more inclusive examination of the structural and functional analysis of microbial diversity than ever before. The recent knowledge of the rhizosphere microbiome, its functions, and their promising biotechnological potential was summarized by several workers (Mendes et al. 2013; Berg et al. 2014). Many studies have shown the importance of metagenomics to the survey of uncultivable microbial communities in different parts of humans, but taxonomic and functional studies related to plants are still limited and rarely emphasized in detail. The main goal of this chapter is to mention the role of the cultivable and uncultivable microbial communities in the maintenance of plant growth, health, and productivity, including the induction of the concept of engineering of plant microbiome for sustainable crop production.

4.2

Modulators of the Rhizosphere Microbiome

Different parameters such as abiotic and biotic factors modulate the diversity of microbes and their composition in the rhizosphere. Hence, the levels to which these factors influence microbial communities are not entirely understood. The abiotic component include climate change, which is caused due to various anthropogenic activities, and biotic components include soil type and variety of pathogens that help in determining the composition of rhizosphere microbiome (Berendsen et al. 2012; Chaparro et al. 2012; Philippot et al. 2013; Spence and Bais 2013). Studies conducted by Caruso (2018) revealed that the soil helps in shaping the mycorrhizal communities in the rhizosphere. The type of root exudates helps to determine the structure of microbial communities and the physicochemical properties of the soil influencing plant health. Climate change causes different abiotic stresses like drought, salinity, and temperature (Prudent et al. 2015; Kashyap et al. 2017). It has been well documented that species of Rhizobium can tolerate dry environments, but their diversity is significantly reduced. However, the scarcity of water affects the nitrogen-fixing ability of rhizobium and the growth and development of leguminous plants (Kunert et al. 2016; Dubey et al. 2019a). Rapid economic and industrial growth has increased anthropogenic activities, a significant cause of pollution and degradation of the ecosystem that significantly affects the microbial community present in the soil. The structure of the indigenous communities of bacteria present in the soil gets homogenized due to the transformation of the forest into farmlands (Rodrigues et al. 2013). Hence, to overcome these harmful effects of climate change, we need to manipulate the rhizosphere microbiome of the plant so that it can withstand extremely harsh conditions (Dubey et al. 2019b).

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Root-Associated Microbiome

Numerous researches were performed previously on plant–microbe interactions with several pathogens. In nature, plants are exposed to several pathogens and severely invaded by many pests and pathogens, leading to great economic loss in agriculture. To protect it, plants can trigger a sophisticated immune response. Furthermore, they recruit more microbes in their rhizosphere that positively affect a plant to improve its growth and boost its immune responses. Unraveling many vital issues regarding how the plant immune system symphonies interact with microbes at the biochemical and molecular levels will need more investigation into these plant–microbe interactions. Several previously performed experiments assessed the microbial diversity associated with different compartments of the plant. Still, only a few microbes are pathogenic though; most of the microbes inhabiting plant-related niches have positive interactions and promote plant survival and fitness (Mendes et al. 2013; Philippot et al. 2013). Outcomes of these researches would help develop imperishable approaches for developing disease resistance in next-generation crops that will help obtain enhanced yields with minimum use of fertilizers or pesticides (Malla et al. 2022). For the first time, scientists unraveled that microbes present in the soil impose physiological constraints on soil pathogens and suppress plant disease (Mendes et al. 2011). Impartially, the microbes present in the soil also communicate a certain degree of hostility to the system across “invaders,” thereby relating the microbial diversity to its innate ability to inhibit or to restrict the survival of exotic organisms (Van Elsas et al. 2012). Plants usually interact with microbes primarily with the help of their roots. The most intense interactions between plants and microbes occur at the rhizosphere, the interface between the plant’s roots and the soil. Plant roots provide various compartments to the microbes at the root–soil interface, such as rhizosphere, endosphere, and rhizoplane, and at this interface, physical and chemical properties of soil change, which influences microbial population (Nihorimbere et al. 2011). However, more habitats are colonized by various microorganisms, and many workers have characterized their activity in association with roots. In the rhizosphere, microbes play key roles in several vital ecosystem processes, such as sequestration of carbon (C) and cycling of nutrients (Singh and Cameotra 2004). Most terrestrial land plants form a close and intimate association with highly complex microbiota, including rhizosphere, phyllosphere, and endosphere. Rhizodeposition fuels an initial substrate-driven community shift in the rhizospheric region, which has the greatest effect on the microorganisms there. These microorganisms connect the genotype of host-dependent fine-tuning of microbial profiles in the selection of endophytes and colonizing different root assemblages (Dubey et al 2019a). The substrate-driven selection also underlies microbial communities at the phyllosphere but exclusively at the immediate leaf surface. Microorganisms colonizing both roots and leaf surface areas contain microbes that allocate indirect protection against pathogens. However, microorganisms present in rhizospheric areas or roots appear to serve as additional host functions through the nutrients acquisition from the soil for the growth of the plant. Roots of the plants

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secrete 5–21% of carbon, which is photosynthetically fixed in the form of soluble sugars, vitamins, purines, inorganic ions, organic acid, amino acids, and some secondary metabolites; the bulk of compounds, like phytosiderophores and nucleosides; and the polysaccharide mucilage produced by root cap cell. Rhizodeposition accounts for about 11% of net photosynthetically fixed carbon, approximately 27% of carbon allocated to roots, and 10–16% of total plant nitrogen. However, these values vary greatly depending upon the species of plants and plant age (Jones et al. 2009).

4.4

Mycorrhiza and Plant Growth-Promoting Rhizobacteria (PGPR)

The association between arbuscular mycorrhizal fungi (AMF) with the roots of the plants constitutes more than 80% in terrestrial plants, different from those selective associations between leguminous plants and between Rhizobium species (Kumar et al. 2015). Phosphorus (P) and nitrogen (N) are the hindering factors for the growth and development of plants. Mycorrhizal symbiosis is the most prime and ubiquitous example of this type of interaction distinguished by the exchange of water and phosphorus for the plant in commerce of carbon for the fungus (Kumar et al. 2010, 2013, 2016). Hence, phosphorus is usually found in the form of strengite and variscite, often inaccessible to the plants even though it is found abundantly in the soil, while calcium is found in apatite in alkaline or acid conditions. Plants absorb phosphate in a soluble form, such as in the form of H2PO4
or HPO4
. Some bacterial species release organic acids that chelate the cations bound to phosphate into the soil (Vassilev et al. 2006). It is estimated that more than 90% of plant species interact with arbuscular mycorrhizal fungi (Bouwmeester et al. 2007; Kumar et al. 2016). The mycorrhizal fungi consume approximately 20% of the carbohydrate products synthesized from plants. Arbuscular mycorrhizae (AM) thrive in the soil in the form of spores till they recognize a specific host plant. Therefore, in exploration for particular roots of the host plants, these spores germinate and spread hyphae through the soil; hyphal branching is stimulated in response to strigolactones present in plants (Kumar et al. 2013, 2016). Fungi form the appressoria after coming in contact with the specific host plant, and with the help of these appressoria, they improve passage to the spaces present between the root cells by using lipo-chito-oligosaccharides (Maillet et al. 2011). Conclusively, inside cortical cells, the fungi form arbuscules. Arbuscular mycorrhizal fungi have recently gathered in greater numbers, due to a combination of genetics and cell biology, as well as the availability of genomic sequences from both mycorrhizal fungus and plants, which has led to increased monitoring. In this context, the advent of new techniques such as omics methods ranging from phylogenomics to metabolomics reveals the communication and variety of symbiotic relationships while also elucidating the role played by various partners in the connection (Kaushal et al. 2020).

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Bacteria that enhance plant growth and provide multiple benefits to the plant are collectively called plant growth-promoting rhizobacteria (PGPR). These bacteria colonize the rhizospheric area and can enhance plant growth and productivity. They are present in significant numbers and positively influence the plant’s growth under specific soil and environmental conditions (Spaepen and Vanderleyden 2011). This can be achieved through direct or indirect interactions with the plant roots. Mechanisms involved in direct plant growth promotion include phytohormone production, atmospheric nitrogen fixation, solubilization of phosphate, and siderophore production (Etesami and Maheshwari 2018), whereas indirect mechanisms of plant growth promotion are mainly related to suppressing soilborne pathogen and deleterious microorganisms by exclusion and antagonism. These mechanisms are attributed more to general plant health than to plant growth promotion by the production of siderophores or antibiotics by the bacteria (Etesami and Maheshwari 2018). Compost and chemical fertilizers formed with the help of PGPR significantly affect the growth and yield of different crop plants. However, with the help of some novel approaches using composted material and blending it with PGPR that can either directly or indirectly facilitate rooting, it is converted into a value-added product such as an effective biofertilizer (Kumar et al. 2016).

4.5

Key Mechanisms Adopted by Host for Recruiting Microbial Diversity

Microbial communities that colonize the host plant benefit from resources derived from the plant and taxonomically create uniform community patterns. Principally, two different, albeit not mutually exclusive, mechanisms might produce such microbiota structures. Plants growing in the soil provide unoccupied niches for intruding microbial strains capable of exploiting the available resources, thus, resulting in stochastic colonization events. On the other hand, plant–microbe co-evolution might provide the basis for a plant-driven selection process, resulting in the active recruitment of microbiota members or at least keystone species that provide functions to the plant host. Root exudates released by the plants are considered the key drivers for establishing plant host-specific microbial diversity in the rhizospheric zone (Marschner et al. 2004). With various chemicals secreted by different parts of the roots into the soil, these chemo-attractants are broadly referred to as root exudates. The importance of root exudates as below-ground defense substances has been underestimated for a long time. These are released behind the root tips, primarily in the elongation zone. Root exudates include thousands of different substances, and a major portion of the carbon (C) is stored as carbohydrates, proteins, sterols, amino acids, and a variety of organic acids; these substances are referred to as water-soluble substances. The differences based on the quantity and availability of carbon in various zones present in the root are specific for different rhizospheric community structures (Yang and Crowley 2000). Consequently, plants secrete a blend of molecules, not just one substance, in response to

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environmental stimuli. This mixture of exudates that are released by roots relies on exterior aspects, such as the height of the plant, age of the plant, soil parameters, and photosynthetic activity of the soil, and these properties vary with species to genus level and also are specific at species or even genotypic level (Semchenko et al. 2014). Microorganisms are recognized as the primary colonizers as the root tip grows toward the soil and penetrates into the deep layers of soil; as continuous root growth occurs, the elongation zone is rarely colonized by microbes present in the soil. Therefore, microbial communities increase a few centimeters rapidly behind the root tips due to volatile root exudates, which act as chemo-attractants for soil microorganisms and are essential for the growth and development of microbial communities. On the other hand, older parts of the root also release some exudates for growth and establishment of microbes that include cellulosic and other recalcitrant materials that form cell wall; these chemicals are sloughed from the tissues present in the root cortex. Differences in the distribution and quantities of these substances, including secondary metabolites and alkaloids, terpenes, flavonoids, and their relative importance in influencing rhizosphere community structure have been observed. Many secrets of the life of microbes and their habitation in the rhizospheric area were recently disclosed due to the latest advancement in microscopic and molecular tools. There are many different components liable for shaping rhizosphere microbiome, but for the variations in community structure, the plant exerts a highly selective pressure as great as that of the soil; hence, microbial communities are actively engaged in various key processes such as the formation of soil, decaying of organic matter, eradication of toxins, and recycling of nutrients like nitrogen (N), carbon (C), phosphorus (P), and sulfur (S). Therefore, these microbes inhabiting the soil find it difficult to maintain the function of soil in both natural and artificially managed agricultural ecosystems. Also, the rhizosphere plays a centrally important role in conducting significant processes that include plant growth, root health, and nutrient recycling. Hence, the microorganism is the key driver for various processes like sequestration of carbon, the functioning of the ecosystem, and cycling of nutrients in terrestrial ecosystems (Liu et al. 2018). These microbes are actively engaged in eliminating various soil-borne plant diseases and promoting plant growth and vegetation changes. Even though the microbiota that resides inside the plant as endophytes can be unraveled into groups of organisms that can be studied in isolation; these distinguishable microorganisms reciprocate in an allied way to the drivers providing support for their functioning and composition found in the rhizosphere. The functioning of the plant-associated microbial community helps plants to ameliorate various diseases and plant growth stimulation by assortment and transportation of various nutrients (Yang et al. 2009; Lundberg et al. 2013). Root exudates play a vital role in plant–microbe interactions. Roots of plants secrete various phytochemical compounds that can mediate different types of interactions, including plant–faunal, plant–microbe, and plant–plant interactions (Huang et al. 2014). Plants use various transport mechanisms to export and release aggregates into the rhizosphere (Badri et al. 2009; Weston et al. 2012). In general, a

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plant root secretes root exudates either as diffusates by passive mechanisms or as secretions by active mechanisms. Most of the organic compounds with low molecular weight are generally secreted by the plants via a passive process, whereas uncharged and polar molecules are transferred directly by passive diffusion. Arbuscular mycorrhizal fungi (AMF) are among the most abundant organisms present on the earth; hence, they represent approximately 5–10% of total global soil microorganism biomass (Lanfranco and Young 2012). Besides these symbiotic interactions, root exudates released by plants are also involved in the commencement of plant and PGPR interactions. The plant growthpromoting rhizobacteria or PGPR enhance the growth of plants by direct and indirect mechanisms. Plant roots release various clues like root exudates that magnetize the diversity of PGPR (Haichar et al. 2008). The carbohydrates and different types of amino acids act principally as chemo-attractants, hence providing strong accuracy, and these root exudates have great potential to convey signals to neighbors. As a result, roots employ a biochemical process to transform signals received from other plants, roots, and soil microorganisms. Although this mechanism is primarily unknown, a recent ecological study has demonstrated that root exudates are crucial for soil interactions (Hinsinger et al. 2009; Sugiyama 2019). Numerous root exudates are known to affect nutrient accessibility, and also, they have the potential to negotiate resource competition. For example, the plant-available concentration of ions, such as phosphorus (P) and zinc (Zn), increases with the exudation of acid phosphatases, protons, and carboxylates (Hawkes et al. 2005; Hinsinger et al. 2009; Sugiyama 2019).

4.6

Mechanism of Action of PGPR

One of the alternatives and evolving strategies used to solve this problem is naturally occurring plant growth-promoting bacteria (PGPB). This eco-friendly microbial community is equally active in stimulating disease management and crop productivity under normal and stressful situations. This approach can be among the most effective approaches for reducing the usage of chemicals, which can undesirably impact human health directly and indirectly (Glick 2014; Dubey et al., 2022a; b; 2021). Several reports show the effectiveness of PGPB for improving plant growth and health. These microbes are well known for their potential to improve plant growth through direct and indirect mechanisms (Fig. 4.1).

4.7

The Direct Mechanism of Action

Direct mechanisms involve the microbial synthesis of phytohormones, such as indole-3-acetic acid (IAA), cytokinins, and gibberellins, by these microbes. Also, these microbes can fix atmospheric nitrogen, and solubilize iron (Fe) and phosphorus (Rosenblueth and Martínez-Romero 2007). Moreover, these microbes have the potential to produce 1-aminocyclopropane-1-carboxylate (ACC) deaminase, which

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Fig. 4.1 Mechanism of action of PGPR

lowers plant ethylene levels because ACC is a precursor for ethylene production (Santoyo et al. 2016).

4.7.1

Fixation of Atmospheric Nitrogen

Nitrogen (N) is one of the essential nutrients present in the atmosphere. It has a key role in enhancing the growth and productivity of the plant. However, about 78% of nitrogen is inaccessible to the plants from the atmosphere. Biological nitrogen fixation (BNF) is the process of fixing atmospheric nitrogen into a soluble form that plants can utilize by a variety of N2 microorganisms present on the earth. BNF is the process to reduce gaseous dinitrogen to ammonia by the nitrogenase enzyme complex (N2 + 8H+ + 16 ATP ! 2NH3 + H2 + 16ADP + 16Pi) and it is well known in rhizobia–legume symbiosis (accounting for up to 460 kg fixed N hectare
1 year
1). Approximately, two-thirds or 66% of the nitrogen is fixed globally by the BNF process, while the remaining nitrogen is synthesized by the Haber–Bosch process (Jiménez-Vicente et al. 2015).

4.7.2

Phosphorus Solubilization

Different types of organic acids may act as metal chelators present in the rhizosphere of the plant. Still, these metal chelators have a profound effect on phosphorus availability compared to the availability of micronutrients. Like iron, phosphorus is another element found abundantly in soil but cannot be absorbed directly from the soil (Mehta and Nautiyal 2001). Strategies to improve phosphorus availability/ uptake can contribute significantly to plant growth because less than 5% of the phosphorus content of soils is bioavailable to plants. Microorganisms with the capacity to solubilize mineral phosphorus are abundant in most of the soils (up to 40% of the culturable population) and can be easily determined by plating on a solidified medium with the incorporation of an insoluble phosphorus form (e.g., hydroxyapatite). Halo formation around colonies indicates the phosphorus

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solubilization capacity of these strains. Well-known bacterial isolates found in these types of soil belong to Bacillus, Pseudomonas, or Penicillium genera (Kumar et al. 2012).

4.7.3

Siderophore Production

Some metal chelators present in the rhizospheric zones of the plants will increase the availability of metals inside the soil. Some micronutrients constituting iron (Fe), copper (Cu), zinc (Zn), and manganese (Mn) are vital to the growth of the plants. These metal chelators establish different types of complexes with soil metals, thus releasing metals that are bounded with soil particles, and hence increasing the mobility and solubility of the metals (Miethke and Marahiel 2007). Iron is often an abundant element present in the soil, but it is not accessible to plants owing to the low solubility of Fe3+ oxides, and plants acquire it with the help of microbes present in the soil. Phytosiderophores have been recognized as including non-proteinogenic amino acids such as avenic and mugineic acids. A mass of bacteria that have plant growth-promotion activities sequesters the Fe3+ present in insoluble form from the rhizospheric soil with the help of siderophores (Miethke and Marahiel 2007; Hider and Kong 2010). Plants uptake iron bound by bacterial siderophores, even though they secrete these siderophores and have a lower affinity for binding iron. This acquisition of iron via microbial siderophores reduces iron availability in the rhizosphere, leading to slower growth of other microorganisms (especially fungi) that may be parasitic to the plant (Loaces et al. 2011).

4.7.4

ACC Deaminase Activity

Ethylene was the first phytohormone described as a fruit-ripening hormone but is now known to have a much broader role in various processes, like stress response in plants, senescence, abscission, and pathogen-defense signaling (Danish et al. 2020). The synthesis of ethylene is highly susceptible to environmental stimulants, including temperature, sunlight, and other plant hormones, in response to various abiotic and biotic stresses (Gowtham et al. 2020). Hence, the production of the ethylene level in plants is also elevated in response to stress. Numerous groups of bacteria evolved with the skill to produce (ACC) deaminase or 1-aminocyclopropane-1carboxylate; for example, Burkholderia spp. can degrade excess amounts of 1-aminocyclopropane-1-carboxylate (Glick 2014; Danish et al. 2020). It is the direct precursor of ethylene in the ethylene biosynthesis pathway. Hence, this can be achieved due to the production of nitrogen and energy as a by-product and the reduction in response to various stresses, which ultimately leads to plant growth promotion. The efficiency of bacteria increases near the plant cells in which biosynthesis of ethylene takes place (Hardoim et al. 2008). Bacteria with ACC deaminase activity frequently provide many benefits and are considered the significant forerunners in sustainable agricultural systems (Glick 2014).

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Signaling of Phytohormones

The phytohormones play a crucial role in the growth and development of the plant, combining both non-remittance developmental pathways and dynamic responses to the environment (Kumar and Dubey 2020). Therefore, phytohormones are considered a key constituent of plant–microbe interactions. Microbial communities produce a variety of phytohormones. Plant responses toward abiotic and biotic stress tolerance, modulation, and regulation of signals exchange (Hause and Schaarschmidt 2009) are involved in the signaling pathway against a pathogen with necrotrophic effects (Stein et al. 2008). Crosstalk mediated by salicylic acid, jasmonic acid, and ethylene activates plant systemic acquired resistance (SAR) and response or induced systemic resistance (ISR); hence phytotoxic microbial communities are reduced. When ethylene is present in a lower concentration, plants can respond to a wide range of environmental stresses. Still, when ethylene concentrations are high, this can lead to plant growth inhibition and even the death of the plant (Kumar and Dubey 2020). Moreover, strigolactones and brassinosteroids are the other compounds identified with hormonal activity (Kumar and Dubey 2020). In the growth medium of many plant-associated bacteria and soil bacteria, phytohormone production is frequently observed; in many cases, the single strain is used to produce different compounds. It has been speculated that phytohormones can be used as signaling molecules between host and bacteria, and the existing crosstalk between auxin (IAA or indole acetic acid) and production of 1-aminocyclopropane-1-carboxylate (ACC) deaminase activity or biosynthesis pathway of ethylene is blocked (Penrose and Glick 2003; Barnawal et al. 2019). Moreover, many bacterial species can also regulate and influence the production of plant hormones. Inoculation of seedlings of Miscanthus plant with a temperate grass endophyte, Herbaspirillum frisingense (GSF30T), stimulates shoot and root growth. Transcriptome analyses revealed that there is regulation of jasmonic acid and ethylene signaling pathway, indicating that the phytohormone activity promotes and modulates plant growth (Straub et al. 2013). A different group of bacterial endophytes were cultured from sweet potato; the cuttings were inoculated with strains of endophytic bacteria that produce auxin and indole acetic acid (IAA), and the cuttings gave rise to roots more rapidly than cuttings that were not inoculated (Doty et al. 2009). It was demonstrated that GSF30T Herbaspirillum frisingense produces IAA in the culture (Rothballer et al. 2008), and it was also concluded that the growth of wheat seedlings increases when inoculated with B. subtilis (due to the production of auxin). Azospirillum spp. is also known to enhance and stimulate plant growth by producing auxin and nitrogen fixation. These bacterial strains can be applied in agriculture fields for sustainable agricultural production. Strain B510 of Azospirillum sp. isolated from surface-sterilized stems of rice significantly increases the yield of rice plants when seedlings are re-inoculated; however, three strains of Pseudomonas enhance the growth and spike length of wheat plants in the field as well as in laboratory conditions (Jiménez-Vicente et al. 2015).

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Indirect Mechanism of Action

Indirect mechanisms include suppression of pathogen infection via antifungal or antibacterial agents. The other indirect mechanisms include assisting plants in acquiring nutrients via phosphate solubilization, nitrogen fixation, and siderophore production. Besides these mechanisms, plant-associated microorganisms improve nutrient acquisition by supplying minerals and other micro/macronutrients from the soil (Hassan 2017). Therefore, isolation and characterization of endophytic bacteria with various properties from unexplored hosts will have many applications to improve plant growth promotion (Santoyo et al. 2016).

4.8.1

Induced Systemic Resistance

Induced systemic resistance has emerged as an essential mechanism by which selected PGPR and fungi in the rhizosphere prime the whole plant body for enhanced defense against a broad range of pathogens, insects, and herbivores (De Vleesschauwer and Höfte 2009). Induced systemic resistance is a generic term for the induced state of resistance in plants triggered by biological or chemical inducers, protecting non-exposed parts against future attacks by pathogenic microbes and herbivorous insects. Plants are in constant contact with a variety of pathogenic microbes (Doornbos et al. 2012). The plants must recognize the invaders and activate fast and effective defense mechanisms against the pathogens to avert these pathogens. Inducible defense responses depend upon the bifurcate innate immune system. One is PAMP-triggered immunity (PTI), which identifies and responds to molecules common to different groups of microorganisms, termed pathogen-associated molecular patterns (PAMPs). The term “PAMP” has been criticized because most microbes are not just pathogenic; therefore, the term microbe-associated molecular pattern (MAMP) has been proposed. MAMPs are sustained among non-pathogenic microorganisms, including endophytes. They are often identified by various toll-like receptors (TLRs) and other pattern-recognition receptors (PRRs) present in plants and animals. Microbe-associated molecular patterns (MAMPs) act as elicitors recognized by plants and trigger MAMP-triggered immunity (MTI). MAMP-triggered immunity, or MTI responses, constitutes the fabrication of the molecules like reactive oxygen species (ROS) and nitrogen that act as antimicrobial compounds and help in signaling (Newman et al. 2014). These molecules activate innate immune responses and protect the specific host from the diseases by determining some conserved non-self-molecules. Bacterial lipopolysaccharides and endotoxins include flagellin, glycoproteins, elongation factor, chitin, and lipoteichoic acid from Gram-positive bacteria, and damage caused by pathogenic infection gives rise to endogenous signals derived from the plant, called damage-associated molecular patterns (DAMPs; Tanaka et al. 2014). Plants generally recognize MAMPs and DAMPs with pattern-recognition receptors (Pieterse et al. 2009). As MAMPs are also conserved in plant-beneficial microbes, they may

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evoke responsive defense such as induced systemic resistance (ISR; Doornbos et al. 2012; Kusajima et al. 2018). Effector-triggered immunity (ETI) is the second branch of plant defense. They respond to virulent pathogenic components secreted directly into the host cell cytoplasm to surpass the protective response and secrete effector protein molecules into the apoplast. PTI and ETI are similar; hence, they involve the procreation of signaling molecules such as salicylic acid, jasmonic acid, ethylene, and/or reactive oxygen species (ROS) and inducing defense-related genes and underpinning of cell walls. Plant cells can recognize and proceed to molecular components of bacteria by using defense-related responses; therefore, the immune system of plants plays a vital role in shaping the framework of the microbiome. Despite the innate immune responses, endophytes can establish themselves inside the tissues of plants in high numbers. Inoculating plants with non-pathogenic bacteria can induce resistance against a broad spectrum of pathogenic organisms below- and above-ground parts. This ISR depends mainly on jasmonic acid and ethylene signaling (Stein et al. 2008). In this way, plants are primed to react more quickly and strongly to a pathogen attack. ISR has been detected for several microbes and their cellular derivative determinants (so-called MAMPs), such as cell envelope elements, flagella, and siderophores (Zamioudis and Pieterse 2011; De Vleesschauwer and Höfte 2009). Wellcharacterized ISR-inducing microbes include several Pseudomonas, Bacillus, and Serratia species and Trichoderma harzianum. Most plant responses have been studied in Arabidopsis thaliana, but ISR has also shown that a partial plant growth promotion can be observed upon inoculation (Pieterse et al. 2014).

4.8.2

Biological Control and Plant Protection

Biological control, or biocontrol, is the process of suppressing harmful or pathogenic living organisms by using other living organisms. Biocontrol has been extensively studied under laboratory conditions and in field situations, leading to several commercial products. Most products are based on Bacillus and Trichoderma strains owing to seed formulation issues, although Pseudomonas-based products have also been commercialized in recent years (Berg and Smalla 2009). Production of Rosmarinic acid (an antimicrobial compound produced by rhizospheric and endophytic bacteria) provides an alternative mechanism for plant protection (Dubey et al. 2020b). Rosmarinic acid provides a dynamic antimicrobial activity against a wide range of microbial communities colonizing the rhizospheric area of the soil, and it was induced in the exudates produced by the hairy root cultures of sweet basil following a challenge by Pythium ultimum (Martinez-Klimova et al. 2017; Naik et al. 2019). Endophytic bacteria inhibit pathogenic quorum-sensing by producing specific antimicrobial products, thereby inhibiting communication, the formation of biofilm, and virulence, without suppressing the growth of bacteria. Endophytic bacteria can also degrade quorum-sensing molecules and suppress biofilm formation in Pseudomonas aeruginosa PAO1 by producing cell-free lysates (Rajesh and

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Ravishankar Rai 2014). Thus, bacterial endophytes can protect the host against harmful pathogens that develop resistance to the plant defenses. Although this quorum-sensing does not impel selective pressure for developing antibiotic resistance, it is another anti-virulence approach for cross-examining drug-resistant bacteria (Kusari 2014).

4.9

Quorum-Sensing and Biofilm Formation

Quorum-sensing is a process of cell to cell communication or regulated expression of genes in response to changes in density and cell population (Kasim et al. 2016). Quorum-sensing has resulted in the regulation of many bacterial genes to limit collaborative performance, such as those involved in biofilm formation, virulence, pathogenesis, and swarming (Choudhary and Johri 2009). Biofilms comprise the complex extracellular matrix of exopolysaccharides and proteins adhering to a solid surface and containing a multicellular assembly of bacteria. The production of these biofilms enables bacterial species to adhere to plant tissues and is an intrinsic element of plant–microbe interactions (Ramey et al. 2005). Transposon mutagenesis of plant-associated Bacillus amyloliquefaciens sp. plantarum FZB42 genes are identified, which are required for the formation of biofilm, bacterial swarming, colonization of roots, and enhanced plant growth in aseptic conditions (Budiharjo et al. 2014). Bacteria present within biofilms are more tolerant toward antimicrobial compounds and are physiologically and phenotypically different from those free-living bacteria (Ramey et al. 2005). Some mutants of Bacillus subtilis that cannot form biofilm cannot protect Arabidopsis from infection caused by bacteria Pseudomonas syringae (Bais et al. 2004). Bacillus subtilis strain 6051 is mutated, resulting in a mutant strain that is susceptible to surfactin synthesis. Surfactin is a lipopeptide with antimicrobial activity. Whereas Bacillus subtilis strain 6051 forms biofilm and releases surfactin and is estimated to be homicidal for P. syringae, the mutant was incompetent as a biocontrol and could not form durable biofilms (Bais et al. 2004). The formation of biofilms can also alter the fate of other compounds present in their proximity due to their physiological response during the absorption of water and organic or inorganic solutes. The plant-associated biofilms are proficient in providing defense from exterior stress, decreasing microbial competition, and providing a protection to the host plant by supporting growth and yield (Auger et al. 2006; Sandhya et al. 2009; Dubey et al. 2020a). Biofilm-producing bacteria also play an imperative role in improving soil fertility and bioremediation (Auger et al. 2006). The study conducted by Wang et al. (2019) used biofilm-forming Bacillus amyloliquefaciens 54, which significantly enhanced drought tolerance by increasing survival rate, relative water content, and root vigor. Furthermore, the biofilm-forming ability of Bacillus amyloliquefaciens improves salt stress tolerance in barley (Kasim et al. 2016), and Bacillus subtilis protects against tomato wilt disease by the formation of biofilm (Chen et al. 2013). Although some studies have been published, there is little direct evidence illustrating

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the role of biofilm formation in protection against abiotic and biotic stresses, especially drought stress (Auger et al. 2006; Chen et al. 2013; Kasim et al. 2016).

4.10

Metagenomics Tools for Plant Microbiome Analysis

High-throughput or next-generation sequencing technology is expeditiously upgraded in speed, cost, and quality. Therefore, it is extensively used to analyze whole prokaryotic communities colonizing different niches (Malla et al. 2019). Here, we have discussed this technology for determining the microbial community’s taxonomic composition and functional role, which occupied different compartments of the plant body. We briefly discussed other high-throughput sequencing platforms and recently developed and commonly used bioinformatics tools applied to metagenomics analysis. The advances in next-generation sequencing (NGS) or high-throughput sequencing have remolded the field of microbial ecology. This type of cutting-edge technology has led to the establishment of a relatively new area, that is, “metagenomics,” which is described as the genomic analysis of genetic material directly recovered from the environmental sample. In this way, it avoids the need for isolation and lab culturing of individual microbial species that act as a significant obstacle to culturedependent methods. Most of the bacterial species colonizing the rhizospheric area are recently unable to be cultured in the labs, and the cultivation-dependent methods are often insufficient for quality analysis of the rhizosphere microbiome (Bell et al. 2014). Many metagenomics computational/statistical tools and databases have evolved in the last decades, and some have been presented in Table 4.1. The conventional approaches were based on isolation and culturing of microorganisms present in the soil, which account for less than 1% of total microbial populations (Torsvik and Ovreås 2002). However, polymerase chain reaction (PCR) amplification of specific genes of interest is widely used in research; this method is known as “shotgun metagenomics” (using 16S rRNA as a marker gene) or “marker gene amplification”. Such strategies allow a much rapid and elaborative generation of genomic profiles of samples isolated from the environment at a very moderate price. Full shotgun metagenomics will enable researchers to sequence the whole genome present within an environmental sample comprehensively. This also provides a means to study uncultivable microbial communities that are otherwise impossible or difficult to inspect. Marker gene metagenomics is a fast and straightforward way to procure a taxonomic or community distribution profile or fingerprint using PCR amplification and sequencing of the 16S rRNA gene, an intact marker gene. The 16S rRNA gene sequencing technique is extensively used to expose various bacterial communities in the biological sample and to construct phylogenetic associations. All bacterial cells possess these genes, which are highly conserved regions that help us know the evolutionary relationships and act as a valuable target for pyrosequencing analyses and PCR amplification of microbial diversity. A thorough inspection of a metagenomics sample requires specific consecutive bioinformatics venture that comprises (i) quality control, (ii) assembly, (iii) detection of

Webbased Webbased

FastQC

EBI

KEGG

GraPhlAn

deFUME

4.

5.

6.

7.

MetagenomeSeq

MetaPath

IMG/M

8.

9.

10.

MetaBAT

Local/ webbased Local

PICRUSt2

3.

Webbased

Webbased

Webbased Webbased Webbased Webbased Local

BiomMiner

2.

Access Webbased

Software MicrobiomeAnalyst

S. N. 1.

Identification of metabolic pathways differentially abundant among metagenomics samples

Binning millions of contigs from thousands of samples Processing, annotation, and visualization of functional metagenomics sequencing data Analysis of differential abundance of 16S rRNA gene in meta-profiling data

Produces high-quality visualizations of microbial genomes and metagenomes

Biological interpretation of genome sequences

To compare functional analyses of sequences

Functional potential of a community based on marker gene-sequencing profiles Annotation

Comprehensive analysis of microbiome data

Applications Comprehensive statistical, functional, and metaanalysis of microbiome data

Table 4.1 List of bioinformatics software for metagenomics data analysis

https://img.jgi.doe.gov/cgi-bin/m/ main.cgi

http://bioconductor.org/packages/ release/bioc/html/metagenomeSeq. html http://metapath.cbcb.umd.edu/

https://bitbucket.org/berkeleyLab/ metabar https://github.com/EvdH0/deFUME

http://segatalab.cibio.unitn.it/tools/ graphlan

http://www.bioinformatics. babraham.ac.uk/projects/fastqc/ https://www.ebi.ac.uk/ metagenomics/ http://www.kegg.jp/blastkoala/

BiomMiner readme – Microbiome Analysis Center (gmu.edu) https://github.com/pic rust/picrust2

Website address MicrobiomeAnalyst

Markowitz et al. (2012)

Liu and Pop (2011)

Van Der Helm et al. (2015) Paulson et al. (2013)

Kang et al. (2015)

Kanehisa et al. (2016) Asnicar et al. (2015)

Mitchell et al. (2016)

Andrews (2017)

Reference Dhariwal et al. (2017), Chong et al. (2020) Shamsaddini et al. (2020) Douglas et al. (2019)

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BioMaS

QIIME

Galaxy portal

mothur

RDP

MG-RAST

MEGAN

11.

12.

13.

14.

15.

16.

18.

Webbased Webbased Local

Webbased Local

Webbased Local

Functional annotation, the phylogenetic distribution of genes, and comparative metagenomics analysis Taxonomic studies of environmental microbial communities Data trimming and filtering, diversity analysis, and visualization Web repository of computational tools that can be run without informatics expertise Data trimming and filtering, diversity analysis, and visualization Data trimming and filtering, and diversity analysis Processing, analyzing, sharing, and disseminating metagenomics datasets Diversity analysis and visualization (needs similarity alignments as input) http://ab.inf.uni-tuebingen.de/ software/megan

http://metagenomics.anl.gov/

http://rdp.cme.msu.edu/

http://www.mothur.org/

https://usegalaxy.org/

http://qiime.org/

http://galaxy.cloud.ba.infn.it:8080

Huson et al. (2007)

Meyer et al. (2008)

Cole et al. (2007)

Schloss et al. (2009)

Caporaso et al. (2010) Goecks et al. (2010)

Fosso et al. (2011)

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gene, (iv) annotation of the gene, (v) taxonomic study, and (vi) comparative study while depositing the sequenced results in the database structured computational repository, which enables advanced management of data, processing of data, metamining, and mining capabilities (Ladoukakis et al. 2014).

4.11

Future Perspectives and Concluding Remarks

The significant societal challenges to produce more food with less fertilizer and agrochemical inputs in crop protection have dramatically increased the awareness of the importance of the root microbiome in plant health for current agriculture. However, with the increasing researches and literature available about plant microbiome, the composition and their prominent roles are advanced in research. Many components will undoubtedly contribute to the rapid expansion of this approach in the future. With the increasing quality of sampling procedure, extraction of DNA, targeted gene amplification isolated from different microbial communities, and others, representing methodological biases will eventually decline in the future. Hence, the broad access of sequence-based analyses allowed by recent development in DNA sequencing techniques makes sequencing of nucleic acids (DNA or RNA) from great numbers of samples possible. Therefore, sequencing cost has declined due to the generation of the massive amount of data vital for the characterization of complicated communities of microbes, which supports the emergence of studies related to the microbiome. This is also dependent on the development of mathematical modeling and advancement in bioinformatics. These advancements in technologies provide most of the robust description of the composition of taxonomic community and phylogeny of microbes, therefore expanding the information available in public databases. By exogenous inoculation of particular microbes and in controlled environmental conditions, it is possible to alter the structure of the microbial community to benefit particular sets of these microbiomes, which leads to increased resistance in plants or harnessing efficiency in the uptake of specific nutrients. In this regard, the development of so-called “microbiome-driven cropping systems” might result in the next revolution in agriculture, resulting in a more sustainable system for plant production.

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From Rhizosphere to Endosphere: Bacterial-Plant Symbiosis and Its Impact on Sustainable Agriculture Gaurav Pal, Kanchan Kumar, Anand Verma, and Satish Kumar Verma

Abstract

Recent findings and advancement in technologies in the field of plant–microbe interactions have led to deeper investigations on the role of soil and endophytic microbial communities in the growth and development of their respective host plants. The process of recruitment of the rhizospheric bacteria inside the host plant tissues through various active and passive passages is also an interesting and established phenomenon. The mutualistic relationship thus developed plays important role in shaping the functionalities of the host plant through different plant growth-promoting mechanisms such as auxin production, nitrogen fixation, and phosphorus solubilization. Nevertheless, these bacteria also enhance the stress tolerance capabilities of the host plant leading to their widespread utilization in sustainable agricultural practices. This chapter focuses on the role of the soil bacterial communities, their recruitment inside the host plants, and their further endophytic life and functionalities. Further, some of the recent applications of seed endophytic bacteria have also been discussed.

5.1

Introduction

Excessive use of chemical fertilizers and pesticides, and climate change have forced the scientific community to find alternative approaches in order to increase the crop productivity sustainably. The interaction of the diverse microbial community in the soil with a number of physiological processes inside the plants has yielded significant observations leading to more intensified research for utilization of this microbial community in agricultural practices (Baker et al. 1997; Berg 2009; Kumar and

G. Pal · K. Kumar · A. Verma · S. K. Verma (*) Centre of Advanced Study in Botany, Banaras Hindu University, Varanasi, Uttar Pradesh, India # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2022 U. B. Singh et al. (eds.), Re-visiting the Rhizosphere Eco-system for Agricultural Sustainability, Rhizosphere Biology, https://doi.org/10.1007/978-981-19-4101-6_5

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Verma 2018). Many rhizospheric microorganisms particularly bacteria have been shown to increase crop productivity. Major functional roles of these bacteria include stimulation of plant growth through enhanced nutrient availability or production of plant growth hormones such as auxins, inhibition of phytopathogens through antibiosis or production of antifungal compounds, tolerance toward abiotic stresses through reactive oxygen species (ROS) production, and improvement of soil health through the bioremediation process (Arshad and Frankenberger Jr 1997; Richardson et al. 2009; Hayat et al. 2010; Pal et al. 2021a; Verma et al. 2021a, b). These functional aspects of beneficial bacteria can be employed in sustainable agricultural practices for improving crop productivity in place of chemical fertilizers. A variety of symbiotic as well as non-symbiotic bacterial species including Rhizobium, Azotobacter, Bacillus, Azospirillum, and Klebsiella have been widely used to enhance the plant production (Burd et al. 2000; Cocking 2003). Such soil-inhabiting bacterial species that contribute in improving plant growth are commonly known as plant growth-promoting rhizobacteria (PGPRs). Effective colonization of the rhizospheric region of the plant by such beneficial bacteria is an essential criterion for their optimal functionality (Lugtenberg et al. 2001). Bacterial colonization in symbiotic bacteria takes place inside the plant cells in specialized structures known as nodules as observed in Rhizobium sp., which occur in leguminous plants (Burd et al. 2000). Mesorhizobium, Bradyrhizobium, Azorhizobium, and Allorhizobium are some of the Rhizobia species that have been reported globally in successfully establishing a symbiotic relationship with the leguminous plants and performing the process of nitrogen fixation (Bottomley and Maggard 1990; Bottomley and Dughri 1989). However, many bacterial species colonize the plant tissues firstly inside the roots followed by shoots and other aerial parts of the plant systematically leading to a more intricate relationship between the two, which further results in better development and stress tolerance capabilities of the host (James et al. 2002; Compant et al. 2005b; Pal et al. 2021b). Such bacterial colonists do not cause any disease symptoms inside the host tissues and are called endophytes (Schulz and Boyle 2006). The recruitment of these mutualists from the rhizospheric region to the inside of the plant is a complex phenomenon and can be achieved through a number of intrinsic and extrinsic factors. The bacterial community present in the soil shows chemotactic movement toward the root exudates released by the plant in the rhizosphere allowing them to efficiently colonize the rhizosphere as well as the rhizoplane (Walker et al. 2003; Bais et al. 2006; Lugtenberg and Kamilova 2009). The plant-beneficial bacteria possessing competitive advantages such as production of lytic enzymes, antibiotics, and siderophores colonize the internal tissues of the plant roots (van Loon and Bakker 2005; Raaijmakers et al. 2002; Haas and Défago 2005). Once inside the plant system, a number of active and passive processes are involved leading to widespread colonization (Compant et al. 2010). However, the community structure as well as number of the endophytic bacterial population varies in response to the stress conditions faced by the host plant (Podolich et al. 2015; Walitang et al. 2018). The utilization of such endophytic species in agricultural systems for improving crop productivity is a more viable and environmentally sustainable approach as these mutualists possess

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important functionalities supporting plant growth and preventing stress conditions (Welbaum et al. 2004; van Loon and Bakker 2005; Lugtenberg and Kamilova 2009; Pal et al. 2019). Plant growth-promoting properties of endophytes include production of growth hormones, 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase activity, enhanced nutrient acquisition, and nitrogen fixation while the synthesis of antifungal compounds, antibiotics, siderophores, lytic enzymes, etc. contributes to the properties of biological control (Hardoim et al. 2008; Chaturvedi et al. 2016; Herrera et al. 2016; Santoyo et al. 2016). These endophytes also provide tolerance to different types of abiotic stress conditions such as salt stress, drought stress, and water stress. The present chapter focuses on the role of microbial communities present in soil as well as inside the plants in shaping modern agricultural practices. PGPRs, their colonization pattern in the plant, and how they form the endophytic community of the host plant are also discussed. Furthermore, this chapter also covers the functional aspects of these endophytes in plant growth promotion and disease prevention (Table 5.1).

5.2

PGPRs and Their Recruitment Inside Plants (Bacterial-Plant Symbiosis)

Modern researches in the field of rhizosphere biology have thrown ample light on the interesting functional roles and mechanisms of associated microbial communities. Reports suggest that these microbial communities could be an important tool that can aid plant as well as soil health. The various biotic activities performed by such microbes make the soil dynamic for nutrient availability and sustainable for agricultural productivity (Koul et al. 2019). The PGPRs that inhabit the rhizosphere (rhizoplane, superficial intercellular spaces, or dead root cell layer) are known as extracellular plant growth-promoting rhizobacteria (e-PGPRs) while those existing in the internal living tissues (nodules, apoplastic spaces of the root cortex, meristematic region, etc.) are called as intracellular plant growth-promoting rhizobacteria (i-PGPRs; Vessey 2003; Gray and Smith 2005). These i-PGPRs are now commonly called endophytic bacteria. Bacterial genera such as Azotobacter, Azospirillum, Agrobacterium, Bacillus, Serratia, Arthrobacter, Pseudomonas, Micrococcus, and Burkholderia are commonly included under e-PGPRs and Rhizobium, Bradyrhizobium, Allorhizobium, Frankia sp., etc. are examples of i-PGPRs (Gray and Smith 2005). The most commonly found genera of bacterial endophytes include Bacillus, Burkholderia, Pantoea, Pseudomonas, Micrococcus, and Microbacterium (Santoyo et al. 2016). PGPRs are known to influence plant growth, increase crop yield, reduce the incidence of disease, and help the plants to cope up with the abiotic stresses (Welbaum et al. 2004; van Loon and Bakker 2005; Lugtenberg and Kamilova 2009). These plant growth-promoting bacteria (PGPBs) can be utilized in agriculture as biofertilizers, biopesticides, or for phytoremediation purposes (Berg 2009; Lugtenberg and Kamilova 2009; Weyens et al. 2009). The inoculation of PGPRs

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Table 5.1 List of crop-plant-associated bacteria with their functional role in plant growth promotion Plant-associated bacteria Kluyvera ascorbata Rhizobium leguminosarum

Crop/plant(s) Canola, tomato Rice

Functional role(s) IAA production, siderophores IAA production

Azotobacter sp.

Maize

IAA production

Aeromonas veronii

Rice

IAA production

Enterobacter sakazakii, Pseudomonas sp., Klebsiella oxytoca Pseudomonas fluorescens

Maize

ACC deaminase activity

Groundnut

Pseudomonas denitrificans, Pseudomonas rathonis Azotobacter sp., Pseudomonas sp. Pseudomonas sp.

Wheat, maize

IAA production, siderophores IAA production

Sesbania, mung bean Wheat

IAA production

Bacillus cereus, Bacillus licheniformis Pseudomonas tolaasii

Wheat, spinach Brassica

IAA production

Bacillus sp., Paenibacillus sp.

Rice

Streptomyces acidiscabies

Cowpea

Achromobacter xylosoxidans

Brassica juncea Brassica juncea, B. oxyrrhiza Cicer arietinum

Pseudomonas sp., Bacillus cereus Bacillus sp.

IAA production

IAA production, siderophores IAA production Hydroxamate compounds Bioremediation of heavy metals (copper) Bioremediation of heavy metals (nickel)

Pseudomonas sp.

Wheat

Bradyrhizobium sp.

Vigna radiata

Pseudomonas

Cassia tora

Bioremediation of heavy metals (chromium) IAA production and phosphate solubilization IAA production and phosphate solubilization IAA production

Pseudomonas, Bacillus

Turmeric

IAA production

ACC, 1-aminocyclopropane-1-carboxylate; IAA, indole acetic acid

Reference Burd et al. (2000) Dazzo et al. (2000) Zahir et al. (2000) Mehnaz et al. (2001) Babalola et al. (2003) Dey et al. (2004) Egamberdiyeva (2005) Ahmad et al. (2005) Roesti et al. (2006) Çakmakçi et al. (2007) Dell’Amico et al. (2008) Beneduzi et al. (2008) Dimkpa et al. (2008) Ma et al. (2009a) Ma et al. (2009b) Wani and Khan (2010) Sharma et al. (2011) Ahemad and Khan (2011, 2012) Kumar et al. (2015) Kumar et al. (2016)

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including Azospirillum, Bacillus, Enterobacter, Klebsiella, and Pseudomonas with seeds/or substrate has been shown to enhance the seedling vigor, production of growth regulators, better tolerance to biotic and abiotic stresses, and improved efficiency in the use of fertilizers (Kokalis-Burelle et al. 2006; Lamsal et al. 2013; Park et al. 2013). However, it has also been shown that PGPRs fail to generate desired response in several cases under field conditions (Compant et al. 2010). This situation might arise because of insufficient colonization (rhizosphere/plant) by the PGPRs, a significant process needed for yielding beneficial traits (Lugtenberg et al. 2001). The process of colonization takes place in response to the root exudates (carbohydrates, amino acids, organic acids, etc.) released by the plant acting as a nutrient source for rhizospheric bacteria (Lugtenberg and Dekkers 1999; Walker et al. 2003; Bais et al. 2006). Bacteria perform chemotactic movement toward the released exudates as a result of which these bacteria colonize the rhizosphere as well as rhizoplane region of the plant root (Lugtenberg and Kamilova 2009). A study demonstrated the colonization of rhizosphere by bacterial cells through gfp or gus labeling of the strains and visualizing them by florescence in situ hybridization (Gamalero et al. 2003). Further extension of the study done with Pseudomonas fluorescens and tomato roots suggested that non-uniform distribution and densities of the strain vary in accordance with the root zone (Gamalero et al. 2004). Reduced chemotactic movement, as well as decreased colonization, was observed when a mutant strain of P. fluorescens lacking cheA gene (responsible for chemotactic movement) was inoculated in the tomato rhizosphere (de Weert et al. 2002). For successful colonization, the PGPBs need to be highly rhizo-competent and production of secondary metabolites including siderophores, antibiotics, and cyclic lipopeptides help the producing strains in having the competitive advantage over other strains (Compant et al. 2005a; van Loon and Bakker 2005; Haas and Défago 2005; Raaijmakers et al. 2008). A number of other determinants such as quorum sensing, bacterial flagella, and production of enzymes are also involved in the process of colonization (Turnbull et al. 2001; Latour et al. 2008; Compant et al. 2010). Following the rhizospheric colonization, numerous bacteria have been reported to colonize the internal tissues of the plant and exhibit plant growth-promoting traits (Hallmann 2001; Compant et al. 2008; Verma et al. 2018; Kumar et al. 2020). It is now a well-established fact that almost all the plants harbor diverse endophytic bacterial communities (Berg et al. 2005). A number of active as well as passive mechanisms can be employed by the bacterial strains for gaining entry inside the host plant (Hardoim et al. 2008). Cracks at root emergence sites and fissures at the lateral root base can act as sites from where the bacterial strains can gain entry inside the host plant (Reinhold-Hurek and Hurek 1998; Goormachtig et al. 2004). Secretion of cell-wall-degrading enzymes, lipopolysaccharides, presence of flagella and pili, etc. are some of the other factors that affect the colonization process (Duijff et al. 1997; Dörr et al. 1998; Krause et al. 2006; Böhm et al. 2007). Once the bacterium enters the root cortex, further colonization takes place with the secretion of cell-walldegrading enzymes, which enable them to pass through the endodermis, allowing

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their entry into the central cylinder (James et al. 2002). Further colonization of the endophytic bacteria takes place either through lumen of xylem vessels or by passing through different xylem vessels via perforated plates from where they can migrate to the above-ground parts of the host plant (Bartz 2005; Compant et al. 2008). Many studies have suggested the presence of endophytic bacteria in flowers, fruits, and seeds as well (Mundt and Hinkle 1976; Misaghi and Donndelinger 1990; Hallmann 2001; Verma et al. 2018.; Kumar et al. 2020).

5.3

Bacterial Endophytes in Plant Growth Promotion and Stress Tolerance

The present working definition of endophytes includes bacterial communities that are present inside the living tissues of host plant asymptomatically for complete or a part of their life cycle (Wilson 1995; Hallmann et al. 1997). Once inside the host plant, the endophytic bacterial community can directly confer the beneficial effects to the plant cell and can easily evade the competition with their rhizospheric counterparts (Santoyo et al. 2016). An established endophytic community inside the tissues of the host plant remains undisturbed by the change in the outside soil environment (Hallmann 2001). Endophytic PGPBs are known to facilitate plant growth and provide better tolerance abilities against different types of stresses. The facilitation of plant growth by endophytic PGPBs can occur by a number of mechanisms including enhanced acquisition of nutrients from the soil (nitrogen fixation, phosphate solubilization, siderophore production), modulation of levels of plant growth hormones (auxin, cytokinin, or ethylene), or by improving the plant fitness through the production of antibiotics, lytic enzymes, volatile compounds, etc. (Ryan et al. 2008; Santoyo et al. 2016; Pal et al. 2021a, b). Production of phytohormones by bacterial endophytes is one of the most commonly employed mechanisms for plant growth promotion (Bloemberg and Lugtenberg 2001; Verma et al. 2021a, b). Many bacterial endophytes have been reported to produce indole acetic acid (IAA), the most common auxin. Nearly 50% of the bacterial isolates from banana trees were found to be producing IAA in the presence of L-tryptophan (Gomes et al. 2017). A study showed that three IAA-producing bacteria isolated from sugarbeet roots when inoculated under gnotobiotic and glasshouse conditions significantly enhanced plant height, fresh weight, dry weight, and number of leaves per plant (Shi et al. 2009). Similarly, cytokinins, gibberellins, and abscisic acid are also produced by different bacterial endophytes but their roles are less commonly understood in the regulation of plant growth (Bhore et al. 2010; Khan et al. 2014; Shahzad et al. 2017). ACC (1-aminocyclopropane-1-carboxylate) deaminase activity of many endophytic bacteria is also known to regulate plant growth by lowering the levels of plant hormone ethylene (Gaiero et al. 2013). In a study, bacterial endophytes (Arthrobacter sp. and Bacillus sp.) isolated from pepper (Capsicum annuum L.) showing ACC deaminase activity resulted in reduced abiotic stress under tested conditions (Sziderics et al. 2007). Similarly, ACC deaminase containing Pseudomonas putida and

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Rhodococcus spp. in peas (Pisum sativum) has been shown to mitigate heavy metal stress conditions (Belimov et al. 2001). Endophytes have shown great potential in the mitigation of abiotic stress tolerance in plants (Lata et al. 2018). Gond et al. (2015) reported increased biomass under salinity stress (1 mole L 1) after treatment with Pantoea agglomerans, which was isolated from teosinte (Zea mays mexicana) roots. They also observed upregulation of aquaporin gene family (mainly ZmPIP and PIP2-1 genes for plasma membrane integral protein) in the treated plants through gene expression analysis. Also, Pseudomonas sp. was shown to induce osmotic stress tolerance in tomato plants under glasshouse and field conditions, as the treatment resulted in increased biomass as well as fruit yield (Sarma et al. 2011). Endophytes have also been known to activate pathogen defense response through a process known as induced systemic resistance (ISR). ISR results in protection of unaffected parts of the plant against a future pathogen or insect attack through a jasmonic acid mediated pathway (Miliute et al. 2015). Endophytic Pseudomonas fluorescens was shown to induce such response against cucumber anthracnose in cucumber plants (Wei et al. 1991). Similarly, another pathogen-induced resistance called as systemic acquired resistance (SAR) mediated by salicylic acid is known to confer resistance to host plants against a wide range of pathogens (Pieterse et al. 2014) (Table 5.2).

5.4

Functionality of Seed-Inhabiting Bacterial Endophytes in Modern Agricultural Practices

Bacterial communities residing inside the seed have shown promising results in plant growth promotion as well as in stress tolerance and are therefore considered as an important alternative in shaping modern agriculture (Hardoim et al. 2008; Kumar et al. 2021). These seed-inhabiting endophytic bacteria face much less competition and share a more close relationship with the germinating embryo than their rhizospheric counterparts, thereby possessing the ability to directly confer their beneficial traits to the developing seedling and contribute to its overall growth and development (Verma and White 2018; Kumar et al. 2020; Pal et al. 2019). However, it has been suggested that seed microbial communities are dynamic and are subject to changes in internal and external environmental factors (Liu et al. 2013). Further, seed status, nutrient composition, germination process, host plant tissue, as well as the genotype of the plant influence the seed microbiome (Mundt and Hinkle 1976; Song et al. 2006; Coombs and Franco 2003; Cankar et al. 2005; Adams and Kloepper 2002). The action mechanism of such bacterial endophytes is similar to the PGPRs such as modulation of plant hormones (auxin, cytokinins, ethylene, etc.), enhanced acquisition of nutrients (nitrogen, phosphorus, iron, potassium, etc.), and providing tolerance against various types of biotic and abiotic stresses. Verma and White (2018) demonstrated the role of indigenous seed bacteria in promoting seedling development of browntop millet (Urochloa ramosa L.), as suggested by increased root–shoot lengths, biomass, and chlorophyll content with respect to the

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Table 5.2 List of PGPRs that have also been reported to control disease in crop plants against various pathogens PGPR strain(s) Bacillus amyloliquefaciens, Bacillus subtilis, Bacillus pumilus Bacillus amyloliquefaciens, B. subtilis, B. pumilus Bacillus pumilus

Crop Tomato

Bacillus pumilus Pseudomonas sp.

Bacillus subtilis, B. pumilus Bacillus cereus Bacillus spp.

Tobacco White clover, Medicago truncatula Pearl millet Tomato Bell pepper

Paenibacillus polymyxa Enterobacter sp.

Sesame Chickpea

Bacillus subtilis Burkholderia sp.

Cucumber, pepper Maize

Azospirillum spp.

Rice

Pseudomonas fluorescens

Banana

Cucumber Cucumber

Biocontrol Tomato mottle virus Cucumber mosaic virus Bacterial wilt Blue mold Acyrthosiphon Kondoi

Downy mildew Foliar diseases Blight of bell pepper Fungal disease Fusarium avenaceum Soil-borne pathogens Maize rot

Rice blast disease Banana bunchy top virus

Reference Murphy et al. (2000) Zehnder et al. (2000) Zehnder et al. (2001) Zhang et al. (2002) Kempster et al. (2002)

Raj et al. (2003) Silva et al. (2004) Jiang et al. (2006) Ryu et al. (2006) Hynes et al. (2008) Chung et al. (2008) HernándezRodríguez et al. (2008) Naureen et al. (2009) Kavino et al. (2010)

uninoculated controls. Further, it was also shown that these endophytes were also protecting the seedlings from fungal phytopathogens, including Fusarium oxysporum, Curvularia sp., Alternaria sp., and Sclerotinia homoeocarpa (Verma and White 2018). In another study, bacterial endophytes from seeds of finger millet (Eleusine coracana L.) were shown to modulate seedling growth and development (Kumar et al. 2020). A study done on abscisic acid producing seed endophyte Bacillus amyloliquefaciens showed a significant increase in plant growth attributes of rice (Oryza sativa) in saline conditions (Shahzad et al. 2017). Pseudomonas spp. strains isolated from seeds of tomato (Solanum lycopersicum) were shown to mitigate cold stress by coding cryoproteins, and reducing membrane damage and ROS levels (Subramanian et al. 2015).

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Conclusion

Soil microflora holds immense potential in shaping modern agricultural practices. PGPRs under optimal conditions can effectively colonize the plant tissues and form a more close relationship with the host plant performing a number of functions that affect the plant growth and development. Plant-associated bacteria fix atmospheric nitrogen into ammonia supporting plant as well as soil health. Moreover, functions like phosphate solubilization and siderophore production also aid in nutrient cycling within the soil. Production of plant growth hormones such as auxin results in changes in the root architecture contributing to improved plant fitness under stress conditions. Antagonistic activity against various phytopathogens and providing tolerance under different types of abiotic stress also make them a more obvious candidate for agricultural applications. Positive outcomes have been reported when these microbial inoculants were used under controlled conditions whether in the laboratory or in the greenhouse. Field trials have also shown promising but heterogeneous results. However, more strategized field trials with the development of more stable and effective microbial consortium as inoculums are needed to be done for ensuring their sustainability in agriculture.

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Arbuscular Mycorrhizal Fungal Symbiosis for Mutual Benefit: More Than Expectation Harsh V. Singh, Udai B. Singh, Pramod K. Sahu, Deepti Malviya, Shailendra Singh, and Anil K. Saxena

Abstract

Arbuscular mycorrhizal fungi (AMF) prevail in most natural terrestrial ecosystems and are widespread geographically having a very extensive host range. AMF form symbiotic relationships with the majority of plant species and play an essential role in ecosystem services, especially plant growth, disease protection and overall soil quality. AMF symbiotic associations are very useful for agriculture and horticulture. It is considered that they have the ability to not only improve crop disease and fertility management but also alter the accumulation of contaminants in plants in various cropping patterns including commercial field and greenhouse crop production. AMF produce glomalin-related soil protein and extra-radical hyphae significantly influence the soil carbon dynamics. The role of AMF is largely overlooked in terrestrial C cycling and climate change. AMF have been recognized as significantly involved in net primary productivity agumentation and further this accumulated additional photosynthets fixed in soil as soil corbon with help of their extended hyphae. AMF colonization also modulates plant defence responses and is found effective in the activation of plant immune responses locally and also systemically against a number of biotic stresses. This chapter highlights the potential of AMF beyond the C sequestration of terrestrial ecosystem concerning the way towards a better understanding of possible AMF mechanisms by which it can be utilized for sustainable agriculture looking the needs of hours the research can be moved forward in a more positive direction.

H. V. Singh (*) · U. B. Singh · P. K. Sahu · D. Malviya · S. Singh · A. K. Saxena Plant-Microbe Interaction and Rhizosphere Biology Lab, ICAR-National Bureau of Agriculturally Important Microorganisms, Kushmaur, Maunath Bhanjan, Uttar Pradesh, India # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2022 U. B. Singh et al. (eds.), Re-visiting the Rhizosphere Eco-system for Agricultural Sustainability, Rhizosphere Biology, https://doi.org/10.1007/978-981-19-4101-6_6

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Introduction

Symbiosis and mutualism among rhizospheric microorganisms and plants are common phenomena going on continuously in the soil. Some microorganisms have strong symbiosis while others have loose, but they have defined niches. Mycorrhizae have a strong symbiosis with the roots of nearly 90% of crops (Pressel et al. 2010). Interactions between plants and microbes for mutual benefits are frequent. They form a symbiosis in general for increased nutritional absorption of plants and/or to cope with adverse conditions. Arbuscular mycorrhizal fungi (AMF) received food and shelter from their host plant. AMF symbiosis can alter host plant physiology, and so their mineral nutrition acquisition capacity is enhanced and the resistance capability of plants is increased for both abiotic and biotic stresses. The resistance capability of plants due to AMF association varied with AMF species associated. It has been studied that AMF colonized plants often produce increased biomass and have increased productivity (Fiorilli et al. 2018). The resistance/tolerance in the plant to soil-borne pathogens due to AMF colonization has been extensively reported (Whipps 2004). AMF are soil-borne fungi and can significantly induce plant resistance to several abiotic stresses due to increased nutrient absorption (Sun et al. 2018). AMF are the group of Glomeromycota order having the colonizing ability of plant roots mostly persisting in cortical cells to form endosymbiosis relationships in nearly 80% of land plants (Ahanger et al. 2014). They form arbuscular structures at the heart of endosymbiosis. AMF take photosynthetically produced carbon compounds in exchange for nutrient supply and provide protection for hosts against pathogens and environmental stress (Sikes 2010). However, the ability of the AMF to adapt to a broad host range, the formation of these arbuscular and the molecular mechanisms involved in the process have not been clarified so far. The name “arbuscular” is derived from characteristic structures called arbuscules formed within the cortical cells of many plant roots as a result of AMF colonization (Smith and Read 2008). Among all mycorrhizae, AMF are the most important and common. First genome sequences of the Rhizophagus irregularis DAOM197198 isolate has been published (Lin et al. 2014). Mycelial networks of mycorrhizal fungi often connect plant root systems over broad areas. These fungi frequently comprise the largest portion of soil microbial biomass (Mahmoudi et al. 2019, 2020). AMF are zygomycetes belonging to the order Glomales. Fossil evidence (Remy et al. 1994) and DNA sequence analysis (Simon et al. 1993) revealed that both AMF and plants are almost more than 400 million years old. AMF have the most peculiar characteristics that occur during the symbiotic relationship with plant roots, it is significantly increases root surface area result of extensive hypha production. These structures help plants to grow under relatively harsh conditions. Several ecophysiological studies have demonstrated that AMF symbiosis is a key component in helping plants to cope with water stress and in increasing drought resistance through altering host root morphology to form a direct pathway of water uptake by extraradical hyphae (Dar et al. 2018). Mycorrhizal symbiosis is one of the most fundamental types of mutualistic plantmicrobe interaction. Being the most common mycorrhizal symbiosis found with

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Ecological fitness Plant Pest

Abiotic stress

Biotic stress

AMF

Nutrients Stress

Ecosystem services Plant Diseases

Fig. 6.1 Common benefits of AMF association to plant

AMF but at the genetic level most of AMF species are not fully characterized (Jiang et al. 2017). AMF are beneficial to the ecosystem by improving soil quality and the carbon cycle. AMF facilitate host plants to grow vigorously under stressful conditions (Begum et al. 2019). AMF mediate a series of complex communication events between the plant and the fungus leading to enhanced photosynthetic rate and other gas exchange-related traits (Birhane et al. 2012). Numerous reports describe improved resistance to a variety of stresses including drought, salinity, herbivory, temperature, metals and diseases due to fungal symbiosis (Ahanger et al. 2014; Salam et al. 2017). An increase in plant root surface area by AMF hyphal network significantly enhances the access of roots to a large soil surface area, causing improvement in plant growth (Bowles et al. 2016). Plants may trade more than 50% of their photosynthetically carbohydrates with AMF and other microbes. AMF play a significant role in soil by mobilizing nutrients available to plants, creating optimized growing conditions, improving soil characteristics and quality and increasing water availability in soil (Fig. 6.1). AMF are thought to have a monophyletic origin in the Ordovician approximately 480 million years ago (Delaux 2017), and they are found in the majority of land plants in most taxa and virtually all ecological niches. Most land plants are facultative symbionts by nature; however, the majority of the plant species have obligate parasitism with the AMF (Graham et al. 2017). On the other end of the scale, some plant taxa, for example, the Brassicaceae and Chenopodiaceae, became asymbiotic and have no interaction with AMF (Brundrett 2004). AMF symbiosis is largely thought to have an association between more than 100,000 plant species and nearly 100 AMF morphotypes. Sexual reproduction in AMF has never been

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observed; however, hyphal fusion (anastomoses) occurs to exchange their genetic material for maintaining new genetic diversity in the population (Chagnon 2014). With the advent of large-scale sequencing approaches, AMF taxonomy and systematics rose to a new level (Spatafora et al. 2016). The advent of new molecular techniques and the results obtained with these modern tools indicate that the diversity of AMF has been underestimated (Lee et al. 2013). Characterization of AMF species on the basis of morphological characteristics is not sufficient, only scattered informations is available (Chen et al. 2018; Savary et al. 2018). AMF offer crucial advantages to the host plant, especially to abiotic stress (nutrient and water) and biotic stress, and protects from diseases and pests (Malhi et al. 2021). Indeed AMF connect whole plant communities of the ecosystem and horizontally transfer plant nutrients. AMF significantly contribute to the uptake of soil nutrients, increase plant biomass and confer on the plant’s improved resistance to stress and pathogens under artificial non-symbiotic condition. Looking at the diverse benefits of AMF to plants and the ecosystem, this review is compiled to collect all aspects of these important organisms for their applicability in sustainable agriculture. The present review highlights on AMF plays a significant role as a primary biotic soil component that is important for efficient ecosystem functions. The compiled findings and information may be used to improve plant AMF symbiotic interaction at molecular levels and these improvements open a new avenue to employ AMF as biofertilizers for sustainable agriculture systems.

6.2

Mycorrhiza

The word mycorrhiza is used to define the association of plant roots and biotrophic mycorrhizal fungi. These mycorrhizal fungi form a network of filaments associated with plant roots. The AM fungi release a number of hormones which lead to stimulate plant growth and accelerate root development and thereby enable plant roots to absorb mineral nutrients from the soil. Based on its morphological characteristics, mycorrhiza is classified into five groups as arbuscular, arbutoid, ecto ericoid, monotropoid and orchid (Wang and Qiu 2006). AMF are the most common variety of mycorrhizal fungi; these are microscopic and branched forms found in the cortical cells of roots (Manchanda and Garg 2007). These AMF are involved in diverse roles from accelerating the nutrient uptake to improving plant development and improving soil health and properties of the soil, thereby influencing the ecosystem. It was known that fungal-host interaction can produce microbe-associated molecular patterns (MAMPs), exopolysaccharides, volatile organic compounds (VOCs), Myc factors and Nod factors (Goh et al. 2014). Moreover, VOCs have demonstrated the ability to modulate root system architecture favouring symbiotic associations and also modulating Nod factor signalling pathway enabling AMF colonization (Maillet et al. 2011). Besides the host specificity the host plant recruit their AMF association or AMF choose their host in the ecosystem, a number of recent studies revealed that the initiation of AMF symbiosis with host

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plant involves varieties of plant genes, hormones and so on and of these strigolactones and fungal derived lipochito-oligosaccharides have been identified as key players (Mohanta and Bae 2015). Additionally, it has been reported that for the development of arbuscules development and AMF infection in legume crops nodulation genes NSP1 and NSP2 and DELLA proteins like SLR1 play key role in AMF infection and nodulation (Jin et al. 2016). To understand the interaction between AMF and the partner plants, identification and characterization of the fungal effectome (means the products of effector condidate genes) are found to be of immense help (Sędzielewska and Brachmann 2016).

6.3

Intracellular Accommodation of AMF

The symbiotic relationship between AMF and the roots of higher plants is widespread. Plants are to be considered to form a complex community with soil microbes and other organisms where plant tissues provide diverse niches for a number of microbes (Kothe and Turnau 2018). AMF are being very long evolutional history (more than 400 million years) to the developed mechanism of the symbiosis (Heckman et al. 2001; Schüssler et al. 2001). This involves plant-derived and fungal signalling molecules that enhance AMF colonization (Gutjahr and Parniske 2013) to form a symbiosis. It includes the extent of adaptation and genetic/metabolic coordination between mycorrhizal partners. Indeed, AMF symbiosis requires a dedicated signalling pathway starting with the root-exudate (strigolactone) acts as signals, which stimulate AMF activity (Kretzschmar et al. 2012). Just before colonization, AMF subsequently secrete a chemical called lipochito-oligosaccharides; host plant sense it and activate a signal transduction pathway. This is shared with root nodule symbiosis and referred to as a common symbiosis signalling pathway (CSSP) (Gutjahr and Parniske 2013). It is well established that generally AMF have very low host specificity. The bidirectional signal exchange involvement during symbiosis is a present-day challenge to our current understanding of communication between both partners. The AMF and their hosts will constantly communicate to establish and maintain the symbiosis. The symbiotic mechanism of AMF and their host comprises many steps: The first step is the searching for the host root. The second step is the penetration of fungi into the host root. The final step is the establishment of mycorrhizal symbiosis. To complete the above-mentioned steps, several molecules (strigolactones) are secreted by the roots and they help AMF to identify their host plants. It also stimulates the growth of AMF and their branching. The AMF interactions are established further with the induction of seven genes (Bonfante and Genre 2010). A multi-level interaction thus will be visible with changed transcriptome, proteome and metabolome patterns. These can be visualized with techniques such as transcriptomics (Nagabhyru et al. 2018), proteomics (Shrivastava et al. 2018) and metabolomics (Rivero et al. 2018; Hill et al. 2018) or combinations thereof (Larsen et al. 2016). Wagner et al. (2015) identified protein effectors as important for the signal exchange between the symbiont and the host. A subgroup of metabolites known as volatile compounds is also addressed for signal exchange (Pistelli et al. 2017). In nature, a partnership between plant and AMF is not

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alone, and additional interactions with bacteria or other fungi will influence the outcome of these associations. These additional interactions in the vicinity of the root are also considered an important mechanism of cross-talk between the partners (Wagner et al. 2016). However, microscopic evidence shows that at later stages the interaction has a very high degree of coordination at the cellular level by the formation of an infection structure that allows cellular invasion (Genre et al. 2008) leads to the formation of the intracellular arbuscules serve as a nutritional (Food storage) interface between the partners (AMF and Plant) (Harrison 2012). The molecular-genetic basis of structure formation is still elusive. The formations of structures is thought to be a prerequisite for AMF infection of host roots and to require signalling through the common symbiosis signalling pathway (Genre et al. 2005). The establishment of AMF is associated with a fundamental reprogramming of the host cell activation of hundreds of genes (Hogekamp and Küster 2013; Calabrese et al. 2017). These genes are thought to be required for intracellular accommodation of the fungus and for coordination of symbiotic functions with their host. AMF spores start germination just followed by signalling process and grow in search of the host root surface by branched fungal mycelia. Finally, they reach host root surface and penetrate and colonized it and establish in the cortical region with finely divided hyphae that ultimately develop into arbuscles (Parniske 2008). A membrane protein (SYMPK) is activated, which codes for a receptor-like kinase with the potential to recognize AMF signals directly or indirectly. Gutjahr and Parniske (2013) reported that a second membrane protein transduces these signals from the cytoplasm to the nucleus by phosphorylating an unknown substrate through its kinase domain. This eventually leads to the regulation of other genes and finally root colonization takes place (Parniske 2008).

6.4

Exchange of Benefits in AMF Symbiosis

Arbuscular mycorrhizal fungi (AMF) in the present-day agriculture is believed to be essential (Sosa-Hernández et al. 2019). AMF are considered as evolved from one ancestral group, an extensive group of fungi that form a mutualistic relationship with most land plant species, including agricultural crops (Brundrett and Tedersoo 2018). AMF are known for their ability to increase plant nutrient uptake and productivity (Smith and Smith 2011). AMF biomass abundance, spore numbers and root colonization levels typically decline with increasing soil depth; however, over 50% of AMF biomass was found below 30 cm (Higo et al. 2013) and from natural plantation it was found up to 8 m depth (De Araujo Pereira et al. 2018). AMF communities are highly relevant components of agroecosystems and found below the plough layer (deeper of six inches) generally are overlooked especially in associated with trees. AMF form finely branched fungal structures called arbuscules which surround the peri-arbuscular membrane of the host and increase the contact surface between the two partners. It has been estimated that it increased the contact area to correspond to a multiple of the entire cell surface (Alexander et al. 1989). Therefore, cells with AMF arbuscules are a suitable site for nutrient exchange. Indeed, the plant host

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expresses many symbiosis-specific nutrient transporters that are thought to mediate mineral nutrient uptake from the AMF (Rausch et al. 2001) and most one is a symbiotic phosphate transporter (AMF genes responsible for phasphate absorption and translocation) (Yang et al. 2012). Vigneron et al. (2018), based on phylogenomic analysis and its orthologs in other land plants, suggest that the AMF-related phosphate uptake pathway represents an early evolutionary innovation. The available information suggests that the arbuscules are the site of the transfer of phosphate from the fungus to the plant and phosphate delivery is the most important benefit of this symbiosis (MacLean et al. 2017) and many other mineral nutrients (Wang et al. 2017). George (2000) also suggests that nutrient elements such as nitrogen, sulfur, and microminerals (i.e. copper and zinc) may be transferred via the arbuscules. Interestingly, AMF-related pathways can also stimulate plant growth and physiology in nutrient-independent ways. Boldt et al. (2011) found that mycorrhizal plants show enhanced photosynthetic capacity. More prominently, the overexpression of a petunia strigolactone transporter (PDR1), which is involved in AMF signalling, has been reported by Kretzschmar et al. (2012). It is sufficient to improve root and shoot growth in the absence of AMF (Liu et al. 2018a, b). AMF and their signalling can potentially increase plant growth in yet unexplored ways. In return for the symbiotic services of the AMF, photosynthates by partner plant receives fixed carbon from the plant. In correspondence to plant-pathogen interactions, carbon transfer has long been thought to carry on in the form of carbohydrates. Indeed, a large body of evidence has demonstrated that AMF can take up and utilize sugars, but only under symbiotic conditions in the roots (Roth and Paszkowski 2017). The work of Tang et al. (2016) indicates that AMF may generate their abundant lipid reserves in spores and vesicles and genomes of two AMF lack a fatty acid synthase complex (Rich et al. 2017). It is thought that the plant host induces several components of fatty acid biosynthesis and processing in mycorrhizal roots indicating that AMF may also receive fatty acids besides sugars. Indeed, it has been confirmed with the recent evidence (Luginbuehl et al. 2017; Brands et al. 2018). AMF lipids are at least partially derived from the host plant; moreover, many aspects of lipid transfer to AMF stay behind to be clarified. A number of soil-inhabiting microorganisms interact with AMF (phosphate solubilizers, free-living and symbiotic nitrogen fixers, antibiotics, plant growth hormone, siderophore and chitinase producers, saprophytes, plant pathogens, predators and parasites). Some soil-inhabiting bacteria possess the ability to produce antibiotics or siderophores which are iron chelators that may act as inhibitors against several plant pathogens or may stimulate plant growth. AMF hyphae, in addition to having enhanced nutrient absorption capability of their host plant, provide an area for the interaction of plants with other soil microorganisms that have an effect on root development and performance (Toljander et al. 2006). These interactions may happen positively or negatively and they may be inhibitory or stimulatory and competitive or mutualistic to each other for the plant. Cordier et al. (1999) reported that AMF establishment in the host rhizosphere changes the microbial population both quantitatively and qualitatively. AMF symbiosis and hyphal net formation can directly or indirectly affect microbial communities in the rhizosphere (Barea et al. 1997). Kloepper (1996) observed that rhizobacteria are known to show a specific ability for root colonization and act as plant growth-promoting rhizobacteria

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(PGPR). Significant progress has been made in estimating the exchange of resources between plants and AMF and their regulation (Walder and van der Heijden 2015). Kiers et al. (2011) demonstrated that the exchange of carbon for nutrients is reciprocally regulated, such that the most beneficial partner receives the most resources in return. These striking results support the idea that biological market dynamics ensure the evolutionarily stable regulation of resource exchange in AMF symbioses (Noë and Hammerstein 1995).

6.5

Significance of AMF for Plants in Natural and Agroecosystems

AMF have a symbiosis with a number of host species in the different ecosystems and considered are not host-specific (Ingleby 2007). The same species of AMF associated with trees can colonize crop species and therefore enhance both tree and crop growth in agroforestry systems. Therefore, the colonized tree species can act as a reservoir of AMF, from which roots of growing crop seedlings can quickly form mycorrhizal associations. Almost all types of soils harbour AMF spores despite the different structural and chemical differences of the cropping fields (Don-Rodrgue et al. 2013). Jean et al. (2018) reported that AMF associated with agroforestry plantations may colonize maize crop plants and they reported that agroforestry plantations harbour AMF inoculum. AMF are one of the most widespread symbiotic fungi colonizing the majority of agricultural plants (Posta and Duc 2020). The effects of AMF on plant growth and physiological elements contents have been widely studied in many species. The ability of AMF to enhance host plant uptake of relatively immobile nutrients, particularly phosphorus (P) and several other micronutrients, has been the most recognized beneficial effect of AMF symbiosis (Smith and Smith 2011). Growth stimulation in the host plant is the result of AMF extending the absorbing network beyond the nutrient depletion zones of the rhizosphere, which allows access to a larger volume of soil. AMF hyphae are much thinner than roots and are able to penetrate smaller pores and uptake more nutrients (Allen 2011). Numerous studies show that AMF (Glomus intraradices) has the ability to solubilize rock phosphate through localized alterations of soil pH and/or by the production of organic acid anions. This alteration through the production of chemicals may act as chelating agents. Additionally, AMF colonization is known to improve plant nitrogen nutrition; however, their role in making N available to plants has not been fully recognized. Uptake of other nutrients, such as Na, K, Mg, Ca, B, Fe, Mn, Cu and Zn, by growing plants is also influenced by AMF colonization (Bucking et al. 2012). The benefit of AMF colonization is not quantified as it depends to a large degree on the environmental conditions. In most natural conditions and under mineral nutrient deficiency coupled with abiotic stress conditions, mycorrhizal plants are thought to have a selective advantage over non-mycorrhizal individuals of the same species. Thus, AMF can potentially promote intraspecific competitiveness and selectively favour mycorrhizal plants. Since numbers of host plant colonized by different species of AMF and similarly AMF species infects numbers of host species, from this point of view it is not clear which

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partner (AMF or host) gets what types of benefits (nutrients, Protection and shelter). The common mycorrhizal networks (CMNs) add an additional level of complexity to the analysis of benefits in mycorrhizal interactions (Jakobsen and Hammer 2015). These common mycorrhizal networks (CMNs) play a critical role in the longdistance transport of nutrients through soil ecosystems and allow the exchange of signals between interconnected plants. CMNs affect the survival, fitness and competitiveness of the fungal and plant species that interact via these networks, but how the resource transport within these CMNs is controlled is largely unknown. A strongly interconnected plant community can potentially gain stability because weaker individuals could profit from mineral nutrient supply from the CMN at the expense of stronger plants that entertain the CMN. In this way, the stronger plants indirectly benefit less competitive plants, thereby attenuating competition among plant individuals. Such “underground socialism” has been invoked particularly in cases where seedlings grew better when they were connected to a CMN that had been established by older plants (Bücking et al. 2016). In the most extreme version of the theme, achlorophyllous plants obtain all their resources, including carbon, from CMN, thereby parasitizing—indirectly—on other plants that supply the network with their carbon (Bidartondo et al. 2002). This can be liked to the transitional evolutionary phase from autotrophy to mycoheterotrophy (Selosse et al. 2017). Aggarwal et al. (2011) also reported that symbiosis of AMF grants benefits directly the host plant’s growth and development. Besides enhancing plant growth and development, they provide a range of benefits from stress alleviation to bioremediation of heavy metals in polluted soils. They may also enhance resistance in a plant against pathogens and increase the plant diversity. Other services provided by AMF in natural and agricultural ecosystems are given in Fig. 6.2.

REDUCTION OF SOIL EROSION AND NUTRIENT LEACHING

ENHANCING NUTRIENTS UPTAKE

HELPS IN SOIL AGGREGATION AND SOIL STABILIZATION

WASTELAND RECLAMATION

ALLEVIATION OF ENVIRONMENTAL STRESS

AMF INCREASED RESISTANCE TO ROOT PATHOGENS ROLES IN ECOSYSTEM SERVICES

AMF IN WEED CONTROL

Fig. 6.2 Significance of AMF in natural and agricultural ecosystem

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Functional Specificity in AMF Interactions with Host Plant

AMF-associated soil microorganism is fundamental for the maintenance of plant health, as it can protect plants from soil-borne diseases and various abiotic stresses. Schweiger et al. (2014) reported that the metabolome is next to diverse biological functions and thus critical for ecological interactions between plants, their enemies, and beneficial microorganisms. AMF alter the plant metabolome by a different way (improving water uptake and nutrition of the host plant) primarily due to increased phosphate supply and acting as an additional sink for plant-derived photosynthates. They are also influencing photosynthesis. AMF are well-known symbiont having agricultural importance, as enhance nutritional values and yields of crops, modulate crop pest and stress resistance and influence global C and P cycling, ecosystem services and primary productivity (Parniske 2008). On the other hand, AMF colonization and formation of extra-radicle hyphae and spores are highly dependent on plant host identity (Thirkell et al. 2019). Indeed, a combinatorial study on mycorrhizal benefits employing a large panel of plant and fungal species from different geographical locations showed that the mycorrhizal growth response ranged from 50% to +50% growth promotion (Kaur and Suseela 2020). The mutualistic potential did not correlate with phylogenetic patterns in either partner. Interestingly, combinations of partners isolated from the same location performed better, indicative of co-adaptation (Wyatt et al. 2014). In agreement with functional specialization, soils with a diverse AMF flora can support more diverse plant communities than if only one or few AMF are present (van der Heijden et al. 1998). Thus, despite the very low host specificity of AMF under laboratory conditions, functional specialization within the AMF community shapes the level of the biodiversity and productivity of plant communities at the ecosystem level. Functional diversity of AMF is given in Fig. 6.3.

6.7

Benefit of AMF to Natural and Agroecosystems

Anthropogenic activities in developing countries like India pose a number of illeffects on the environment. These activities increase accumulation of heavy metals and other organic contaminants into the different eco-system, causing ill effect to environment, contaminates water bodies and accumulate in soil and finally accumulates in crops (Rai et al. 2019). Continuous release of exceeding amounts of contaminants such as geochemicals, agrochemicals and industrial chemicals containing heavy metals pose risks to food safety and human health have much considered nowadays and urgent needs felt for formulating strategies to reduce their effects (Rai et al. 2019). Besides playing an important role in crop and soil health improvement, AMF also reduce the accumulation of contaminants in plants. AMF symbiosis and its role in the reduction of contents of organic contaminants and the underlying mechanisms have been studied in detail. Results of experimentation indicate that AMF widely occur in contaminated sites with organic chemicals. AMF improve plant tolerance to organic contaminants and enhance crop growth,

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Enhance Adaptation ability of host plant to survives in harsh environmental conditions Secretion of Hormones and antibiotics beneficial to host plant

Enhance in nutrient up taking

AMF functions

Protection of plant against other pathogens by induction of ISR

Protection of host plant against root pathogens by production of hyphal network

Mobilization of major and micro nutrients

Fig. 6.3 Functional diversity of AMF symbiosis in natural and agricultural ecosystem

leading to increased biomass of the crops. Besides improved nutritional supply to the host plant, AMF interactions also provide other benefits to plants, such as improved drought and salinity tolerance (Augé et al. 2015) and disease resistance (Pozo and Azcón-Aguilar 2007). In the last few years, the mechanisms responsible for the increased plant tolerance to stress have yet to be fully elucidated (Szczałba et al. 2019). Several benefits received by AMF symbiosis and the mechanisms in ameliorating organic contaminant residues in crops can be easily understood with following points: (1) AMF improved mineral nutrition and water availability, (2) they alleviated oxidative stress results of contaminants, (3) they enhanced activities of enzymes related to contaminant degradation, (4) AMF structures like mycelia and arbuscles accumulate and capture of contaminants, (5) glomalin-related soil protein (GRSP)-triggered changes in bioavailability of contaminants, (6) AMF also stimulate the activity of contaminant degrading soil microorganisms, (7) improved soil structure; and (8) reduced pesticide application as act as biopesticides and biofertilizer. (9) Reduced weed population because of inhance plant growth. AMF may provide several benefits to the ecosystem (Chen et al. 2018). A number of studies and reviews have highlighted the AMF contributions to phytoremediation of soils polluted with heavy metals (Wang et al. 2017) and organic contaminants (Rajtor and Piotrowska-Seget 2016). AMF can enhance phytoextraction efficiency by increasing the accumulation of contaminants in plants, particularly in aerial parts (Cabral et al. 2015). In general, the plant faces two major stresses: abiotic related to water, nutrient and environmental stress and the other is biotic, which includes stresses rendered by various pathogenic microorganisms

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causing diseases and other pests. AMF association mitigates this stress by employing various mechanisms induced by themselves or induced by host plant in response to AMF. Thus AMF contributed in so many ways to host plants and play a significant role in sustaining the ecosystem. Besides the above-mentioned attributes, AMF can also provide other ecological functions by influencing the soil microbial community and chemical environment of the mycorrhizosphere. AMF symbiosis may play a significant role in stabilizing soil aggregates by the production of glomalin and conferring plant tolerance to several abiotic stress (Li et al. 2013; Chitarra et al. 2016) and biotic stress (van der Heijden et al. 2015).

6.7.1

AMF Association for Mitigation of Biotic Stress in Cropland Ecosystem

In addition to the benefits of nutrient cycling and acquisition to plants, AMF-associated plants showed increased tolerance to abiotic and biotic stresses (Rivero et al. 2018; Campo et al. 2020). AMF priming is suggested as the mechanism underlying mycorrhiza-induced resistance (Balmer et al. 2015; Sanmartín et al. 2020). AMF symbiotic plants have more resistance to several pathogens. AMF symbiotic plants scale up defences in a faster and more efficient manner, representing a phenomenon known as defence priming (Martinez-Medina et al. 2016; Mauch-Mani et al. 2017). Out of several defence responses, the most fascinating cellular defence responses against pathogens are the deposition of β-glucan polysaccharide callose. This sugar polymer strengthens plant cell walls against attackers, blocks their entrance and provides the plant with additional time to activate subsequent defence mechanisms from their cascade if needed. Mustafa et al. (2017) demonstrated that AMF symbiotic plants infected with Blumeria graminis show increased papillae formation at penetration sites. AMF can trigger callose accumulation in wheat following chitosan infiltration (Pérez-de-Luque et al. 2017). Sanmartín et al. (2020) reported that B. cinerea infection in tomato plants can be challenged with priming of Rhizoglomus irregularis. Roth and Paszkowski (2017) found that several sugar transporter genes belonging to the SUT family (SUT1, 2, and 4) and SWEET family, some invertase genes (LIN6) and sucrose synthases have higher levels during AMF symbiosis. Plants colonized with AMF act by various mechanisms to combat biotic stresses (Fig. 6.4).

6.7.2

Effects of AMF on Plant Defence and Disease Resistance

Mycorrhizal roots often exhibit intense colonization both intercellularly and intracellularly and sometimes it can be reached more than 90% of the total root length. AMF colonization mostly depends on the right fungal partner and is very much influenced by the environmental conditions; however, fungi have to produce chitin as a molecular signal to activate defence mechanisms of plants (Boller and Felix 2009). Indeed all pathogens usually produce inhibitors of defence known as

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Resistance to Pathogens AMF hyphal network resistance to soil pathogens Defence Genes activation

AMF barrier to soil borne pathogen

Transcription factors

Compeon for space and nutrition

MAMP triggered Immunity

AMF hyphal proliferaon and spores formaon

AMF

Plant colonized with AMF

Fig. 6.4 AMF strategies to mitigate biotic stress in plant under crop land ecosystem

effectors. It has been predicted that AMF also have numerous effectors in the genomes (Sedzielewska Toro and Brachmann 2016; Kamel et al. 2017). Only a few of them have been functionally analyzed (Kloppholz et al. 2011). In contrast, AMF symbiotic plants often exhibit increased disease resistance (Cameron et al. 2013). AMF colonization in nature improved plant health due to better nutrition acquisition, or a systemic induction of the defence status, well recognized as systemic acquired resistance (SAR). In addition, AMF, or other microbes associated with their mycelium, can directly interfere with rhizospheric pathogens.

6.7.3

Mechanism of Plant Disease Reduction by AMF

The AMF symbiosis involves several mechanisms in the management of plant biotic stress. A numbers of studies and reports suggested that AMF followed various strategies to combat biotic stress (Dehne 1982; Krishna and Bagyaraj 1984; Reid 1990) and the mechanisms involved are as follows: (a) Production of lignifications, plant roots become thicker and production of other polysaccharides which in turn restrict the entry of root pathogens. (b) It creates a mechanical barrier in the host root which hinders the pathogen penetration and subsequent spread. (c) By producing and accumulating a sufficient quantity of metabolites, which provide resistance to the host tissue against plant pathogen invasion.

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(d) Stimulating flavonoid wall infusions which prevented lesion formation by the pathogen Fusarium oxysporum. (e) Increase amount of phenol reduce pathogen growth. (f) Producing antifungal and antibacterial antibiotics and toxins. (g) Colonizing the host plant root and rhizosphere and showed competition with the soil-borne pathogens for the uptake of essential nutrients. (h) Stimulating the rhizospheric microbial activity and creating competition in the root zone that resulted in preventing the pathogen to get access to the roots. (i) Roots colonized by AMF enhanced the activity of actinomycetes antagonistic to root pathogens. (j) AMF helps plant in absorption due to extended hyphal growth. (k) Changing the amount and type of plant root exudates favouring the pathogen growth. Other workers reported that resistance to fungal diseases was found with inoculation of AMF. Inoculation of G. mosseae significantly reduces pink root disease caused by Pyrenochaeta terrestris. Abdalla and Abdel (2000) reported that G. mosseae protects peanut plants from infection by F. solani and Rhizoctonia solani. Plant resistance/tolerance to biotic stresses can be enhanced drastically through AMF inoculation (Saghir et al. 2010).

6.7.4

AMF Association for Mitigation of Abiotic Stress in Cropland Ecosystem

Drought stress is one of the most devastating abiotic factors among the different forms of abiotic stress, threatening crop growth and productivity worldwide (Guo et al. 2020). Both salt and drought stresses share some common properties and generally result in impaired key physiological functions in living organisms such as fungi (Daffonchio et al. 2015). Salinity, drought and high temperature have become serious problems in many regions, not only because of a higher risk to public health and the environment but also because of negative effects on the yield. Salinity characterizes as hyperosmotic stress is one important stress, posing a water deficit that is comparable to a drought-induced water deficit (Daffonchio et al. 2015). The application of AMF for the mitigation of such salinity can be achieved (Plouznikoff et al. 2016). With the multiple benefits that AMF confer to their hosts, they hold great promise for application in crop production under various conditions. Most agricultural crops are hosts for AMF and can therefore potentially benefit from inoculation with AMF. Some AMF species were isolated from Arabian arid regions and deserts: F. mosseae, Claroideoglomus etunicatum, R. fasciculatus, G. aggregatum, Diversispora aurantia, D. omaniana, S. africanum and undescribed Paraglomus species (Dhar et al. 2015; Symanczik et al. 2015). Indeed, many studies have shown that the application of commercial AMF inoculum benefits crops under agricultural conditions (Weber 2014). Numerous studies have shown that AMF can increase plant health and yield (Rouphael et al. 2015; Hijri 2016). One important

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Increase in water uptake Increase soil water retention properties

Oxidative stress decreasing

ROS and MDA reduction

Glamilin related soil protein increase

Reduction in antioxidant enzymes

Increase in stable soil aggregation

Reduction in proline, sugars and osmolytes

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Regulating structural opening of host stomata.

Enhance in photosynthesis by increasing chlorophyll

Production of phytohormones MeJA IAA ABA,

Enhnce root growth and mycelia net

Increase in water retention

Increase in nutrient uptake

Direct

Water stress

Indirect

AMF

Nutrient stress

Fig. 6.5 AMF strategies to mitigate abiotic stress of plant

aspect of this is the promotion of root system development (Gutjahr and Paszkowski 2013). Zou et al. (2020) suggested that AMF can regulate physiological and molecular responses to tolerate drought stress, and they have a strong ability for coping with drought-induced oxidative damage through the production of the oxidative burst in the arbuscule-containing root cortical cells. Similar to plants, AMF modulate a fungal network in enzymatic (e.g. Superoxide dismutage SOD encoding genes (GmarCuZn SOD) from Gigaspora margarita and copper-zinc superoxide dismutase Cu/Zn-SOD gene (GintSOD1) from Glomus intraredices) and non-enzymatic (e.g. GintMT1, GinPDX1 and GintGRX1) antioxidant defence systems to scavenge ROS. Plants also respond to mycorrhization to enhance stress tolerance via metabolites and the induction of genes. Li et al. (2020) also reported that AMF inoculation alleviated the toxic symptoms under moderate salt levels (100 and 150 mM). Greenhouse study conducted on potatoes clearly indicated that AMF inoculation helps in the mitigation of phosphorus and nitrogen uptake and water use efficiency (Liu et al. 2018a, b). Chakraborty and Saha (2019) in their reviewed paper indicated that AMF are the most important component in the mitigation of several abiotic stress. AMF also help plants to cope with heavy metals, diseases and pathogens. AMF symbiosis mitigates these stresses through various mechanisms, which are increased hydromineral nutrition, ion selectivity, gene regulation, production of osmolytes and the synthesis of phytohormones and antioxidants (Diagne et al. 2020). Different mechanisms and strategies adopted by AMF for the mitigation of abiotic stress are given in Fig. 6.5.

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Significance of AMF in the Managed Ecosystems of Different Climatic Zones

AMF are associated with a majority of plants in natural habitats and are playing a significant role in important ecological services from nutrient mobilization and acquisition to the improvement of soil structures. AMF are an important component of all ecosystems and their diversity and distribution mostly depend on the cop communities, soil types and climatic factors of the ecosystem. These symbiotic associations are found with most crop plants including cereals, vegetables and fruit trees and well recognized components of sustainable agriculture (Chen et al. 2018). Gao and Guo (2010) reported that AMF are present in almost all the ecosystems. Vieira et al. (2019) concluded that the AMF community assemblages in tropical mountains are related to the heterogeneity of habitats of these ecosystems. Different land use patterns affect the diversity and distribution of AMF species in ecosystems. Jansa et al. (2006) observed that AMF functional traits differ considerably among and within species, meaning that the functional properties of a mycorrhizal community depend on its composition. Melo et al. (2020) observed that AMF species varied with the type of crop species in the ecosystem. Deforestation is a major problem in an arid ecosystem. Replantation by adaptation of agroforestry in the degraded land through Government along with local bodies is now executing to restore natural habitat. These are the measures to stabilize degraded and eroding surfaces. Newly established trees are very vulnerable to abiotic stresses. This critical phase can be overcome with mycorrhizal inoculation of the trees before planting. Mycorrhizal inoculation significantly increases the growth and health of young trees, thereby increasing their fitness and survival after planting (Sellal et al. 2017). Another interesting example is stabilizing sand dunes by planting the drought-tolerant mesquite tree (Prosopis juliflora), which increases mycorrhizal communities in sand dunes (Moradi et al. 2017)

6.9

Commercialization of AMF

AMF have multifaceted characteristics that raised opportunities for their commercial application. It has been observed that the AMF-related markets considerably grew well during the past decades, with increasing numbers of actors, products and market volume (Vosatka et al. 2008). Commercial AMF products are readily available and targeted at the general public and agricultural industry. In the market, mycorrhizal formulations are sold in granular, powder, liquid and tablet forms. Dry products comprise dusts, granules and wettable powders. Dusts have a particle size ranging from 5 to 20 mm and contain about 10% inoculums of an organism by weight. These products include inert carriers such as charcoal, lignite, clay minerals (perlite, vermiculite and bentonite), starch polymers, dry fertilizers and ground plant residues (Pal et al. 2016). Since the 1990s, the number of companies selling mycorrhizal products in the markets. If we consider globally, the main players are coming from North America, Europe, Asia and Latin America. In the domain of the Americas, the

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main markets include the United States, Canada, Mexico, Brazil, Argentina, Colombia and Chile. The Asia region is mainly dominated by India, followed by China. The Indian market itself has seen an outstanding growth during the last decade mainly due to the involvement of organizations such as The Energy and Resources Institute (TERI). In general, the AMF are being produced by small- and medium-stakeholders and cover local and regional markets. The European market represents one of the leading markets for mycorrhizal biostimulants. In Europe itself, the number of firms producing and selling AMF products has increased from less than 10 firms in the late 1990s to more than 75 firms in 2017. The largest domains of application include gardening and landscaping, horticulture, agriculture, forestry, golf courses, recultivation of degraded land, roof plantings, soil remediation and research. The cost of mycorrhizal inoculation for professional uses at an agricultural scale is considerably low, with an estimated investment of 135$ per hectare in the case of potatoes in the United States (Hijri 2016). Apart from pure AMF inocula, many products include mixed fungal inocula, sometimes in combination with ectomycorrhizal fungi or with plant growth-promoting rhizobacteria.

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Rhizodeposits: An Essential Component for Microbial Interactions in Rhizosphere Madhurankhi Goswami and Suresh Deka

Abstract

Rhizodeposits are essential rhizosphere-associated constituents synthesized by plants that support various biological and physiochemical activities in soil. They significantly influence microbial root colonization capacity, multiplication of rhizosphere microorganisms, soil microbial activity, soil health and secretion of organic bioactive compounds. Root exudates are a group of vitally important compounds with multifarious functions and are released from the living plant roots. They are a complex group of substances secreted by plant roots consisting of low molecular and high molecular weight constituents. The root exudate composition reflects the opposing-associating trait of plants towards rhizosphere microorganisms. These rhizosphere microorganisms produce a wide range of antibiotics that provide a defence to the host plants against a number of phytopathogens. The root exudates, produced as a part of the rhizodeposition process, exert a direct impact on the biogeochemical cycling of carbon and nitrogen. They help in modulating organic matter decomposition in soil by altering the microbial communities involved in the decomposition of soil organic matter and also affect the soil nitrification process. Root exudates are well known for their activity as chemoattractant and signalling molecules for successful M. Goswami Environmental Biotechnology Laboratory, Resource Management and Environment Section, Life Sciences Division, Institute of Advanced Study in Science and Technology (IASST), Guwahati, Assam, India Life Sciences Division, Department of Molecular Biology and Biotechnology, Cotton University, Guwahati, Assam, India S. Deka (*) Environmental Biotechnology Laboratory, Resource Management and Environment Section, Life Sciences Division, Institute of Advanced Study in Science and Technology (IASST), Guwahati, Assam, India # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2022 U. B. Singh et al. (eds.), Re-visiting the Rhizosphere Eco-system for Agricultural Sustainability, Rhizosphere Biology, https://doi.org/10.1007/978-981-19-4101-6_7

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interactions between plant and rhizosphere microorganisms. Thus, the current chapter will elaborate on the various roles of root exudates in plant-microbe interaction and rhizosphere functioning, the mechanism of root exudates and the molecular insights of the root exudation process.

7.1

Introduction

7.1.1

Rhizosphere: A Dynamic Ecological Niche Space for Complex Microbial Interactions

The ‘rhizosphere’ which refers to the nutrient-rich region of the soil surrounding the plant roots is a metabolically active and diversely rich hot spot for microorganisms, considered to be the most complex ecosystem on Earth. The various biological and chemical processes occurring in the rhizosphere soil is solely influenced by the roots. The rhizosphere represents the most complex and metabolically active region of the soil which controls plant-microbe interactions. The complexity of the rhizosphere region varies with the variation of plant genotypes and also with the age and architecture of plant roots. Apart from the domain, the width of the rhizosphere region also depends on the plant species. The rhizosphere microzone differs from the bulk soil (commonly known as edaphosphere) in terms of increased microbial population and metabolic activity and also due to higher accessibility of plant root exudates. Over the years, efforts have been made to restructure and regenerate the definition of rhizosphere so as to depict three regions, which include the endorhizosphere, the rhizoplane and the ectorhizosphere. The endorhizosphere, as the name suggests, refers to the apoplastic space between the cells and includes the root cortex and the endodermal cells. The rhizoplane refers to the intermediate region or the root surface adjacent to the roots. The ectorhizosphere is the topmost zone of soil that surrounds the plant roots (De-la-Pena and Loyola Vargas 2014). The rhizosphere microbiome is a complex, highly dynamic microbial assemblage under the control of a number of environmental factors. Soil and plant genotypes are equally crucial in shaping the rhizosphere microbiome via recruitment of soil microorganisms from the bulk soil. Even during a pathogen attack, the host plant actively takes part in selecting a specific group of microbial cells from the rhizosphere microbial community to control and inhibit the infection. This is how disease suppressiveness is triggered in soil despite the presence of virulent soil pathogens. Disease suppressiveness is solely due to the involvement of soil microbial communities and the intense microbial activity in the rhizosphere zone which is activated with an onset of a disease (Mazzola 2002). The recruitment of specific antagonistic microorganisms from the rhizosphere during pathogen invasion was studied and elaborated by Mavrodi et al. (2012). For example, under circumstances of pathogen attack in wheat plants, that is, Gaeumannomyces graminis var. tritici (under irrigated conditions) and Rhizoctonia solani (under dry conditions), the major soil-borne pathogens attacking wheat plants, the wheat rhizosphere recruits

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2,4-diacetylphloroglucinol (DAPG) producing pseudomonads and phenazine producing pseudomonads to suppress the growth of take-all pathogens G. graminis var. tritici and R. solani. Thus, under conditions that favour pathogen attack, the host plant recruits antagonists from the rhizosphere microzone to suppress the ill effects of pathogens on host plants. The rhizosphere soil is an indication of a high microbial population, increase microbial diversity and metabolic activity. The diversity and functionality in the rhizosphere soil are mainly owing to the production of root exudates due to the secretion of organic carbon by the roots (Bakker et al. 2013). Plants act as the main source of organic carbon in soil due to physiological and biochemical plant processes such as litterfall, plant senescence and the C loss from the plant roots. These plant-derived C inputs constitute approximately 0.5–10% of the total C fixed in the soil. The soil microbes get chemotactically attracted to the C containing compounds secreted by the plant roots leading to their survival and proliferation in this carbonrich environment. These root-derived C containing compounds are collectively referred to as rhizodeposits (Farrar et al. 2003).

7.2

Rhizodeposits: A Vital Component for Plant-Soil Linkage

Rhizodeposits are grouped into different classes based on their composition, mode of release or function. They include substances like root exudates, actively released secretions like proteins, mucilage, lysates, secondary metabolites and inorganic molecules, shedded border cells, root cap cells and the ageing root tissue (Bowsher et al. 2018). The rhizodeposits released into the soil are differentially used by diverse components of the soil community that includes the rhizosphere microbial communities and other residing soil fauna. They behave specifically towards a different group of soil microorganisms resulting in their attraction or repulsion (Fig. 7.1). The composition, superiority and quantity of root exudates being released by the host plant vary between the type of plant cultivar, plant developmental stage and also on environmental factors such as soil type, soil pH, temperature and the residing microbial communities. This chapter will spotlight the importance of root exudates, based on the large body of literature, with the aim of unveiling the mechanistic insights of root exudation patterns and the potent roles of root exudates in different dimensions.

7.2.1

Root Exudates: A Multifunctional Compound of the Rhizosphere Microzone

Root exudates are considered to be the most essential among the rhizodeposits for plant-microbe interactions and rhizosphere microbial community structure. The living roots of plants release plant photosynthates that include sugars, carbon compounds, inorganic ions, metabolites and amino acids as root exudates (Badri

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Fig. 7.1 Interaction of rhizodeposits with beneficial or pathogenic rhizosphere soil microorganisms resulting in the stimulatory or inhibitory effects

et al. 2013; Chaparro et al. 2013). The sugars that are present in the root exudates include monosaccharides, disaccharides and five-carbon sugars; amino acids include arginine, asparagine, glutamine, aspartate and cysteine. Root exudates also consists of organic acids such as benzoic acid, acetic acid, ferulic acid, ascorbic acid and malic acid. Apart from the aforementioned constituents, root exudates also contain phenolic compounds and some high molecular weight compounds such as auxin, gibberellin, flavonoids, fatty acids, enzymes, nucleotides, alkaloids, polyacetylenes, tannins, steroids, terpenoids and vitamins (Hayat et al. 2017) (Table 7.1). Root exudates are classified into two groups: the high molecular weight (HMW) compounds such as proteins, terpenoids, vitamins and polysaccharides and low molecular weight (LMW) compounds such as amino acids, sugars, phenols, organic acids and other plant metabolites. The HMW compounds are not easily utilizable by soil microorganisms but make up the majority of C present in the root exudates,

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Table 7.1 Different potential roles of root exudates and the compounds detected in root exudates (adapted from Dakora and Phillips 2002; Haichar et al. 2014) Component in root exudates Amino acids and phytosiderophores

Organic acids

Sugars and vitamins

Functions Nutrient source, acts as a chemoattractant and helps in chelating poorly soluble mineral nutrients such as Fe, Al and Ca phosphate

Nutrient source, acts as a chemoattractant, helps in chelating poorly soluble mineral nutrients and induces the expression of nod gene, soil acidifiers and Al detoxifiers Replaces phosphates from rocks making them available for microorganisms, promotes microbial and plant growth

Phenolics, inorganic ions and gases

Nutrient source, chemoattractant molecules, microbial growth promoters, nod gene inducers as well as nod gene inhibitors, Al detoxifiers, chelators of poorly soluble mineral nutrients and resistance

Proteins and enzymes

Catalysts for P release from organic molecules, biocatalysts for organic matter transformations and plant defence

Detected components in root exudates a- and b-alanine, proline, Asparagine, valine, threonine, aspartate, tryptophan cysteine, ornithine, cysteine, histidine, glutamate, arginine, glycine, homoserine, isoleucine, phenylalanine, leucine, -Aminobutyric acid, lysine a-Aminoadipic acid, methionine, serine and homoserine Citric, glutaric, oxalic, malonic, malic, aldonic, fumaric, erythronic, succinic, ferulic, acetic, butanoic, butyric, syringic, valeric, rosmarinic, lactic, glycolic, trans-cinnamic, piscidic, formic, aconitic, pyruvic, vanillic and tetronic acids Glucose, deoxyribose, oligosaccharides galactose, biotin, maltose, thiamine, ribose, niacin, xylose, raffinose pantothenate, rhamnose, riboflavin, arabinose and fructose Liquiritigenin, luteolin, daidzein, 40 ,7dihydroxyflavanone, genistein, 40 ,7dihydroxyflavone, coumestrol, 4,40 -dihydroxy-20 -methoxychalcone, eriodictyol, 40 -7-dihydroxyflavone, 3,5,7,30 -tetrahydroxy4’methoxyflavone, Naringenin, isoliquiritigenin, 7,30dihydroxy-40 -methoxyflavone, umbelliferone, (+)- and ()- catechin Acid/alkaline, phosphatase, amylase, invertase, protease, PR proteins, lipases, beta-1,3-glucanases

while the LWC compounds are readily utilizable, more diverse and are accompanied by a wide array of significant functions. The root morphology serves as an important criterion in influencing the overall make-up and composition of root exudates. The ageing portions of the plant roots were known to exude more of organic acids, while the root tips of primary and lateral roots secrete more of amino acids (McDougall 1968; Rovira 1969). Each part of the plant roots is specialized for the secretion of different compounds as part of root exudates (Frenzel 1957, 1960). For instance, the meristem or the root apex secretes glutamic acid, valine, leucine and phenylalanine as root exudates while the outer

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layers of the root cap cells and root hair cells are specialized in the secretion of mucilage. Mucilage secretion can also occur due to degradation of the root epidermal cells. Aspartic acid is secreted overall by the entire root system. The zone following the root tip region is considered to be the primary site for root exudation in plants (Badri and Vivanco 2009). Root exudation by the plants is due to the tremendous root pressure at the growing root tips in order to push their way through the soil. The root exudates mediate multipartite interactions in the rhizosphere region. They behave as a food source attracting neutral, beneficial and pathogenic soil microorganisms. As a response, the host plant introduces compositional modulations that cause the recruitment of beneficial soil microbes, thereby inhibiting/suppressing the pathogenic ones to avoid the flourishing of the non-beneficial microbial community in the rhizosphere microzone as well as defending the plants from pathogens (Zhang et al. 2009). Root exudations occur by both active and passive transport systems wherein LMW compounds are transported by the process of direct passive diffusion. The movement of these compounds depends on cell membrane permeability, intracellular fluidic pH and polarity of the molecules that are being exuded by the plant roots while the HMW compounds are transported via membrane-bound transporter proteins including the ATP binding cassette (ABC) transporters (Badri et al. 2009; Yuan et al. 2018). Additionally, substrates such as indoles, pyrrolidines, quinolines and isoquinolines belonging to different classes of alkaloids produced by plants; flavonoids and phenolic acids that refer to plant-derived phenolic compounds and antimicrobials are transported from the living roots to the rhizosphere via multidrug and toxic compound extrusion (MATE) active transporters by using ion electrochemical gradient (Weston et al. 2012). The movement of exuded root secretions in soil depends on diverse factors such as the quantity of root exudation, the nature of root secretions, the receptiveness of the compounds by the soil microorganisms for microbial assimilation and degradation, the nature and quantity of clay in the soil and the total water load of the soil. The zone that extends up to 1–2 mm from the root is considered the distance that is travelled by the root exudates. This rhizosphere microzone observes the maximum microbial load due to the high influence of root exudates that comprises sugars, organic acids and amino acids (Rovira 1969).

7.2.2

Factors Influencing Root Exudation Pattern

There are a number of factors that influence the exudation of compounds from the living plant roots. Soil moisture, plant biotype, microorganisms residing in the vicinity of the roots, damage to the living plant roots and the prevailing environmental conditions influence and modulate the root exudation pattern in plants. The quality and quantity of root exudation vary among plant species. For instance, both the root exudates of wheat and barley plants contain sugars but the difference in both the exudates occurs in the case of certain sugars such as galactose,

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glucose and rhamnose, which is due to species variation. Variations in root exudation among species may be due to fluctuations in the distribution potential of the photosynthates which serve as a basic substrate for root exudates. Apart from plant biotype, plant root architecture also influences the exudation pattern as well as the distribution capacity of photosynthates. The morphological characteristics of roots including the surface area of roots, the root branching type, root tip density or the size of the root system determine the rate and extent of the distribution of photosynthates in soil. The absorbing roots that include the primary roots exhibit higher physiological activity than the xylem and phloem vessels present in the plant roots. These roots help in the exchange of materials across the plant roots. These differences in the architecture of the absorptive roots among species or within species, that is, the overall root architecture, play a decisive role in determining the root exudation rates (Yang et al. 2020). Additionally, the leaf habits also exhibit a strong influence over the root exudation pattern of plants. For instance, the studies undertaken by Sun et al. (2017) and Wang et al. (2019) have observed that there occurs higher exudation in deciduous trees than the evergreen trees, which was due to the differences in the leaf habit of both the plants. Furthermore, environmental conditions and soil characteristics exert a strong relationship on the root exudation pattern of plants through direct or indirect effects. In consideration of environmental conditions, soil warming or an increase in soil temperature plays a crucial role in root exudation patterns. Several studies have investigated its influence on root exudation. Husain and McKeen (1963) have reported that the exudates obtained from strawberry plants grown at 20–30  C contained higher amounts of amino acids than those grown at 5–10  C. But the influence of soil warming on root exudation varies from plant to plant. For example, Schroth et al. (1966) observed that root exudation from cotton and bean plants was higher at a temperature of 37  C, whereas it was lower in case of pea plants. In the case of pea plants, the exudation rate was observed to be higher at 27  C. A similar pattern was observed for Vicia faba plants where the exudation of tannins and phenolics showed a profound increase at 30  C, which was comparatively low when grown at 4  C (Bekkara et al. 1998). An increase in temperature influences the root exudation pattern not only quantitatively but also qualitatively. Reports suggest that differences in the release of exudates due to temperature variations were due to alterations in the permeability of the cellular membranes or changes in cellular metabolism. Lower metabolic energy at lower temperatures allows substances to leak out of cells (Hale et al. 1971). Light intensity is one of the other factors responsible for exudation variations in plants. It modifies the exudation rate of secondary metabolites because of alterations in the biological phenomenon of photosynthesis. For instance, a few studies have reported that root exudation strictly depends on diurnal rhythms, which means an increase in root exudation during the light periods while declining during dark periods (Watt and Evans 1999). For example, Hughes et al. (1999) have reported that under light conditions the root exudates of Alnus glutinosa (L.) contain more of flavonoid content than the root exudates that were produced during dark conditions. As for tomato and subterranean clover plants, a similar root exudation pattern was observed. Clover plants grown

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under diurnal light exuded more serine, glutamic acid and a-alanine as part of root exudates than those growing under shady (60%) conditions. In the case of tomato plants, levels of aspartic acid, glutamic acids, phenylalanine and leucine in exudate were high during light periods, which were reported to be reduced by shading (Rovira 1969). Soil moisture significantly influences the exudation patterns in plants. As in the case of high soil moisture, there is less availability of oxygen in the soil, which results in hypoxia. Under hypoxic conditions, there occurs a shift in the respiration process from aerobic to anaerobic. This shift in respiration results in the accumulation of ethanol, lactic acid and alanine at phytotoxic levels in the plant root system (Rivoal and Hanson 1994). The plants defend themselves from the harmful effects of accumulated ethanol and lactic acid by secretion of a wide range of metabolites as part of root exudates (Xia and Roberts 1994). Any damage whether physical or chemical to the living plant roots can cause significant changes in root exudation patterns. The extent of influence on root exudation is more pronounced for physical damage to roots than chemical ones. Physical damage to the plant roots can occur during digging, trenching or roto-tilling within the root area of the existing plants, whereas chemical damage occurs due to the excessive application of chemicals to the plants. There are studies suggesting that physical damage can cause a sharp increase in the release of amino acids by 73–120% in comparison to the intact, undamaged root system (Ayers and Thornton 1968). In addition to amino acids, physical damage to plant roots can also significantly influence carboxylate exudation in plants (Tiziani et al. 2020). In reference to chemical damage, Martin (1957) has reported that there was increased exudation of root exudates (scopoletin) from oat and wheat roots (C14-1abeled organic compounds) (McDougall and Rovira 1965) when immersed in distilled water in comparison to the nutrient solution. Distilled water is hypotonic while a plant cell is hypertonic. So, when a plant cell is placed in distilled water, water moves from the outside of the cell to the inside, resulting in cell swelling which leads to increased membrane permeability. Thus it can be observed that both physical and chemical damage influences root exudation patterns in plants although the influence shown due to physical damage was more pronounced than that of chemical.

7.2.3

Mechanism of Root Exudation and Genes Involved

Root exudation is a biological process involving multiple mechanisms facilitating transport of soil C to the living plant roots and its release to the surrounding soil. The C produced in the source organs in the phloem is translocated by a specialized mechanism known as Munch’s pressure-driven mechanism that drives the phloem mass flow by use of a pressure gradient in the phloem (Liesche and Schulz 1930). It works principally based on the turgor pressure difference that exists between sink and source organs. During phloem unloading, the low molecular weight compounds are diverted to the phloem pericycle where they are unloaded and eventually move out of the phloem pole pericycle. The high molecular weight compounds like protein

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compounds remain restricted to the phloem pole pericycle. In no time, the low molecular weight molecules move out of the plant roots to the surrounding soil environment. In order to do so, these molecules need to move across the plasma membrane to reach the apoplast. The plasma membrane is permeable to small, gaseous molecules, while it is impermeable to larger, charged as well as uncharged polar molecules (e.g. glucose) (Canarini et al. 2019). The small polar molecules and the uncharged molecules are transported through simple passive diffusion using the permeability nature of the lipid membrane as a criterion. The movement of smaller molecules through the lipid membrane is solely dependent on the electrochemical gradient between the source and the sink. The electrochemical gradient helps in the translocation of the molecules from the cytoplasm of root cells to the vicinity soil. The larger molecules pass through the membrane by interacting with specific transmembrane proteins, which is known as facilitated diffusion. These proteins help in transiting the molecules by forming small pores through the lipid bilayer or phospholipid bilayer membrane (Sasse et al. 2018). The efflux of the larger compounds such as sugars, amino acids and organic acids can also take place through specific efflux pumps and channels. A few of the transporters have been characterized for amino acids such as Usually multiple acids move in an out Transporter (UMAMIT), Cationic Amino acid Transporter (CAT), Lys His Transporter (LHT), Glutamine Dumper transporters (GDU) (Pratelli et al. 2010; Besnard et al. 2016). Similarly, for the transport of sugars, transporters like Sugars will be eventually exported as Transporter (SWEET), Sucrose Transporter (SUTs) and Monosaccharide Transporters (MUTs) (Hennion et al. 2019) and organic acid transporters such as Multi-drug And Toxic compound Extrusion/citrate Transporters (MATE) and Aluminum-activated Malate Transporters (ALMT) (Wu et al. 2018) have been characterized. Excretion of high molecular weight metabolites by roots can also take place via vesicular transport (Badri and Vivanco 2009). The newly synthesized secondary metabolites are transported by the vesicles to other storage compartments or the plasma membrane for efflux. This process of exudation of metabolites involving vesicles is known as exocytosis. In some cases, the allelopathic compounds secreted by the plant roots are cytotoxic to plant cells. These allelopathic compounds are separated from the cytosol by membrane-bound vesicles by a process known as vesicular trafficking. Vesicular trafficking and exocytosis are known to be involved in combating attacks by plant pathogens (Grotewold 2001). Ion channels are responsible for the secretion of carbohydrates and carboxylate ions such as malate and oxalate. These exuded compounds are transported across the lipid membrane through a transport mechanism mediated by proteins. The most widely studied transporter is the aluminum-activated-malate transporter (ALMT). They consist of a group of proteins, responsible for several physiological plant processes like exudation of organic acid in the presence of toxic Al3+ ions in the soil, conferring aluminium tolerance in plants under aluminium stress conditions (Sharma et al. 2016). For instance, the organic acid (OA) anions were known to render Al3+ resistance to plants under Al toxicity, but their exudation from the plant roots involves a cascade of events. The cascade starts with Al3+/H+ activating

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unknown receptors. Activation of the receptors results in an increase of cytosolic Ca2+ ions which activate the calcium sensor proteins or calmodulin. The activated calmodulin protein binds to the glutamate decarboxylase enzyme converting it from an inactive form to an active form. The activated form of glutamate decarboxylase enzyme converts glutamate to ɣ-aminobutyric acid, which is involved in the regulation of expression of ALMT1 activity in Arabidopsis thaliana plants. In Arabidopsis, Al-tolerance genes such as AtALMT1, AtMATE, ALS3 and different H+ tolerance genes are regulated by zinc finger protein sensitive to proton rhizotoxicity1 (STOP1). STOP1 is considered a core component for controlling Al and H+ tolerance in Arabidopsis, while STOP2 regulated by STOP1 protein confers only H+ tolerance in Arabidopsis due to low expression of AtMATE and ALS3 genes. In addition to these, there are a few other factors like calmodulin-binding transcription activator2 (CAMTA2) that is involved in the regulation of expression of the AtALMT1 gene (Kobayashi et al. 2014). Just like in Arabidopsis, in the case of Oryza sativa, the ART1 gene encodes for a transcription factor that is involved in the regulation of 31 downstream genes implicated in Al tolerance. Briefly, Al tolerance in rice is basically due to the involvement of a number of genes that are associated with the process of detoxification of Al at different cellular levels (Tsutsui et al. 2011). The downstream genes that are regulated by ART1 were characterized to be STAR1 and STAR2 (SENSITIVE TO AL RHIZOTOXICITY1) encoding ATP binding and transmembrane domain of a bacterial-type ATP-binding cassette transporter, Nrat1 (Nramp Al transporter 1), located in the plasma membrane of the root cells and functions as a transporter for trivalent Al into the plants which is essential for the prior step of final Al detoxification, OsALS1, CDT3 and OsFRDLA1 encoding an Al-induced MATE transporter. The ALMT transporters are not the only ones that confer stress tolerance in plants but there are MATE active transporters that also confer tolerance in plants against different stresses (Liu et al. 2009). MATE transporters play a vital role in the transport of a wide variety of molecular substrates, hormones and secondary metabolites (Takanashi et al. 2014). These are the independently activated transporters that confer stress tolerance to plants and are actively involved in citrate exudation. Secretion of root exudates can also take place via proteins located in the root plasmatic membrane through an active transport mechanism. The active transport mechanism consists of two classes of membrane transporters, namely, ABC and MATE transporters. The root exudation from the living roots involving proteins occurs in three different situations depending on their specificity: transporters that are involved in the secretion of various metabolites, membrane transporters that are involved in translocation of different metabolites to the rhizosphere soil and the unique and highly specific transporters that are involved in the exudation of compounds from plant roots (Jones and George 2002; Orelle et al. 2018). The ABC group of transporters are considered the primary transporters while the MATE transporters are considered the secondary active transporters, and this is due to the fact that the former utilizes the energy from ATP (adenosine triphosphate) hydrolysis while the latter uses electrochemical gradient from the transportation of compounds across the membrane (Weston et al. 2012).

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Root Exudates Mediating Belowground Interactions

Root exudates play a vital role in the root rhizosphere region. Through the exudation of a wide range of compounds as root exudates, the plant roots can structure the soil microbial community and regulate their existence in the immediate vicinity of the roots. Moreover, root exudates can help the soil microbiota in coping up with herbivores, stimulating the process of plant-microbe symbioses, modulating the soil physical and chemical properties and playing a pivotal role in the growth suppression of different pathogenic microorganisms and competing for plant species (Nardi et al. 2000; Walker et al. 2003).

7.3.1

Root Exudates Mediating Plant-Microbe Interactions

From the previous literature, it is well known that plant roots are the most potent source for the recruitment of soil microbes. These soil microbes help in promoting the growth of the plants, protecting the host plant from diverse plant pathogens and increasing plant tolerance to abiotic stress conditions. The predominant factor that helps the host plant to recruit rhizosphere soil microbes are the root exudates which commute with the rhizosphere-residing beneficial microbes while inhibiting the non-beneficial soil microbes.

7.3.1.1 Root Exudates: An Essential Chemoattractant for Microbial Host Root Colonization Plants exude high levels of C as root exudates that behave as chemoattractant for bacteria. Most of the motile bacteria direct their movement in response to these chemical gradients, a bacterial response known as chemotaxis, for initiating a communication between the plant roots and the soil bacteria and colonizing the root region of the host plants (root colonization). The chemotactic response of bacteria increases their root colonization efficiency in the rhizosphere. The various molecules exuded by the plants help in initiating a positive bacterial chemotaxis towards different host plants leading to root colonization (Brencic and Winans 2005). Bacterial chemotaxis is initiated by the binding of a signalling molecule to a chemoreceptor. This transmembrane chemoreceptor which is responsible for bacterial chemotaxis is also known as methyl-accepting chemotaxis protein and consists of a number of domains. The transmembrane consists of a periplasmic or cytosolic ligand-binding domain, cytoplasmic region consisting of HAMP (histidine kinase, adenyl cyclase, methyl-accepting chemotaxis protein [MCP] and phosphatase) linker and a signalling domain. The ligand-binding domain is responsible for binding extracellular compounds. Once the ligand binds itself to the binding LBD, autophosphorylation of the histidine kinase CheA gets altered, which in turn transfers the phosphoryl groups to the response regulator CheY. Subsequently, the generated CheY-P permits its interaction with the flagellar motor to control cell swimming or tumbling to ultimately mediate chemotaxis (Feng et al. 2018). Existing literature reported bacterial chemotaxis towards various molecules exuded by host

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plant roots as root exudates mediated by specific chemoreceptors in establishing plant-microbe interaction following host root colonization (Webb et al. 2014; Allard-Massicotte et al. 2016). Root colonization is one of the most important factors that aids in plant-microbe interaction. Root colonization is considered a key process that controls plant growth and induces systemic tolerance against different biotic and abiotic stresses (Sachdev and Singh 2018). The metabolites and the other organic secretions as a part of root exudates favour microbial colonization of root surfaces. Root colonization occurs when several groups of soil bacteria form microcolonies or biofilms on root surfaces. Biofilms are an assemblage of microbial communities embedded in a matrix of extracellular polymeric compounds (Bogino et al. 2013). The extent of biofilm formation varies between different root regions. In accordance with the previous literature, the depth and thickness of microbial biofilms are higher in the apical region of the roots than in ageing or mature root regions. This is due to the fluctuations in the composition of the root exudates and nutrient availability at the root plane or specific secretion of antimicrobials from the root tip (Rudrappa et al. 2008).

7.3.1.2 Root Exudates as Signalling Molecules The organisms in the rhizosphere region interact with each other as well as plants via chemical communication established in the rhizosphere microzone. The plants secrete a wide array of metabolites as a response to altered gene expression, which is a result of signalling molecules secreted by the rhizosphere microorganisms. Overall, plants produce a compositionally diverse array of more than 100,000 different low molecular mass natural products known as secondary metabolites. In this chapter, we will explain a few of the molecules that are involved in legumerhizobia, plant-AMF and actinorhizal plant-Frankia interactions. Rhizobia Bacteria belonging to the Rhizobiaceae family produce flavonoids and non-flavonoid signalling molecules that play a significant role in symbiotic interactions. The symbiotic interaction between any strain of bacteria belonging to the Rhizobiaceae family and legume is the result of a molecular interaction based on the signal molecules produced and secreted by both the associated partners involving a succession of recognition events. Initially, the interaction starts with the exudation of signal molecules by the host plant that expresses the genes involved in the process of nodulation. Flavonoids are a group of plant secondary metabolites that are well known for their activity in plant-microbe interaction. They are synthesized via the central phenylpropanoid pathway and the acetate-malonate pathway. Flavonoids consist of two benzene rings connected by a three-carbon linking chain. They consist of two aromatic rings which are synthesized by different biosynthetic pathways. The flavonoids are categorized into different subgroups based on their molecular structure including flavonols, flavones, flavanones, isoflavonoids, chalcones, catechins, anthocyanidins and dihydroflavonols. There are several studies that have reported its

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role in in vitro nodule formation process using reporter genes (Shaw et al. 2006). The legume roots are known to secrete flavonoids into the surrounding soil. The quantity and concentration of the flavonoids increase with the presence of Rhizobium species in the soil. The flavonoid molecule behaves as a signalling molecule expressing the nod genes in rhizobia. The expressions of nod genes are responsible for the synthesis of Nod factors that initiate the nodulation process (Haichar et al. 2012). The Nod factors are lipochitooligosaccharides that act as signalling molecules triggering a sequence of events in host plants such as root hair curling or shepherd’s crook, infection thread formation to allow the entry of rhizobia to the host root cells and nodule development (Cullimore et al. 2001). The process of nodule formation is regulated by both rhizobia and the plant and involves mechanisms that are controlled by two factors, that is, nodule numbers and nodule position (Sasse et al. 2018). The existing literature suggests that Nod factors induce certain flavonoids to initiate nodule formation through their action as auxin transport inhibitors. By inhibiting auxin transport inhibitors, there involves a local accumulation of auxin at the nodule initiation site initiating the development of nodule primordial. Similarly, the non-flavonoid molecules are also involved in inducing the expression of nod genes. There are several studies that documented the activity of various non-flavonoid molecules in inducing the expression of nod genes. For example, trigonelline and stachydrine from alfalfa seeds (Phillips et al. 1992), aldonic, erythronic and tetronic acid (Gagnon and Ibrahim 1998), xanthones (Yuen et al. 1995), vanillin and isovanillin from wheat seeds (Le Strange et al. 1990) can induce expression of nod genes in S. meliloti by activating the regulatory NodD protein, nod genes in Mesorhizobium loti, Rhizobium lupini, and Sinorhizobium meliloti, B. japonicum, Rhizobium sp. respectively Frankia Actinorhizal symbiosis is a type of symbiotic interaction occurring between actinobacterium Frankia and dicotyledonous plants. The symbiotic interaction between the two partners initiates with the infection process. As in Rhizobium, ‘shepherds crook’ is also observed in Frankia, but unlike Rhizobium Nod factors, the extracellular deforming factors in the case of Frankia are quite different both structurally and functionally (Bagnarol et al. 2007). As in the case of Rhizobium/ legume interaction, the main factor is the host-derived flavonoids that help the rhizobia to interact specifically with their hosts, and similar is the case with Frankia. The root hair curling in Frankia is initiated on interaction with the host root filtrate. There are few studies that have correlated the strain specificity in MyricaceaeFrankia symbiosis with root phenolics. The main root exudates that were affected by Frankia inoculation are phenols, flavonoids and hydroxycinnamic acids. The existing literature suggests that flavonoids determine the microsymbiont specificity as the host plant adapts to their secondary metabolism in accordance with the compatibility status of bacterial strains (Popovici et al. 2011). There are studies that reported that Frankia inoculation to host plant A. glutinosa activates the genes coding for phenyl ammonia lyase (pal) and chalcone synthase (chs), involved in flavonoid biosynthesis. Similarly, the study by Auguy et al. (2011) revealed that

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Frankia interacts with the tropical tree Casuana glauca Sieb. ex Spreng. and results in the activation of eight Casuana glauca genes coding for enzymes involved in flavonoid biosynthesis. Arbuscular Mycorrhizal Fungi (AMF) Arbuscular mycorrhizae are found to colonize the majority of land plants. Mycorrhizal colonization of plant roots is mediated by controlled exudation by the plant roots and sensing of specific secondary metabolites released by the roots. During plant root colonization, the roots communicate with the mycorrhizal association in a complex way. The mycorrhizal fungi obtain a substantial fraction of soil C as a primary source of energy for the metabolic activities in the soil while at the same time benefitting the plants by delivering soil nutrients in return. One of the crucial steps in AMF development in plant roots is the formation of extraradical hyphae induced by signal molecules exuded by plant roots that initialize AMF-induced symbiosis. The signalling molecules secreted by the plant roots as a result of AMF interaction are known as strigolactones. Strigolactones are known as branching factors exuded by plant roots. They are well known for their activity in stimulating fungal hyphae branching in symbiotic AMF. Strigolactones also help in signalling directional growth of AMF towards roots. Most important, strigolactones are considered an important signal molecule for the establishment of the AM symbiosis (Akiyama and Hayashi 2006). Strigolactones are synthesized from the carotenoid pathway and any alterations in the carotenoid mechanism affect strigolactone synthesis which ultimately affects AMF-host interaction. Recently it was reported that strigolactones play a crucial role even at a later stage of the AMF-plant interaction, when the fungus is already established in the root (Steinkellner et al. 2007).

7.3.1.3 Root Exudates as Carbon Cycling Activator and Nitrification Inhibitor The exuded materials from the plant roots contain high amounts of C compounds that directly impact the rhizosphere microbial population. Root exudates can provide the rhizosphere microorganisms with precursors that are essential for phytohormone synthesis. Studies reported that plant exudates also contain higher quantities of aminocyclopropane-1-carboxylic acid (ACC) which serves as the main source of carbon and nitrogen for the rhizosphere microbes. This was shown by acdS expression by root exudates. Living plant roots also exude certain sugars such as glucose and sucrose that are involved in exopolysaccharides production, which is an essential step in microbial biofilm formation (Haichar et al. 2012). For instance, on growing Paenibacillus polymyxa in a culture medium containing a high concentration of sucrose, a high level of levan production was observed. Levan is a naturally occurring fructan present in many plants and microorganism species. High levels of sugar induce the expression of gene sacB involved in levan synthesis. Thus, it was clearly understood that the exuded sucrose from the root apex of wheat roots in the rhizosphere ecosystem can easily induce the expression of the P. polymyxa sacB gene (Bezzate et al. 2000). These Exopolysaccharides play a pivotal role in legume-

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rhizobia interactions via taking part in microbial biofilm formation around the plant roots. Since EPS can be produced at high levels of sugar concentration (that is either glucose or sucrose), it points out to facts that (a) root exudates contain a high concentration of these molecules and (b) in the presence of gene expression inducer bacteria may produce EPSs with low glucose or sucrose concentrations. Plant roots exude a wide array of organic substances as a part of root exudates. The organic compounds exuded by the roots were reported to accelerate the process of decomposition of soil organic matter (SOM) with the help of soil-dwelling, rhizosphereassociated microorganisms. The increased solubilization of soil nutrients depends solely on the activation of rhizosphere microbial activity by labile C released by roots. The existing literature suggests that some of the primers like root exudates, even at meagre amounts, can stimulate SOM turnover, which increases nutrient availability, especially nitrogen or phosphorus to plants (Jones et al. 2004; Cheng et al. 2014). The nitrification process is a key step in the global nitrogen cycle that links the oxidation of ammonia to the loss of fixed nitrogen in the form of dinitrogen gas brought about by specific nitrifying microbial activity. The process involves converting a non-utilizable form of N in the soil to a simple, readily utilizable form that contributes significantly towards plant productivity and environmental quality. The existing literature demonstrated the importance of using recombinant luminescent bacterial strains (Nitrosomonas europaea) to monitor nitrification inhibitors released from plant roots (Subbarao et al. 2007). Among the cereals, legume crops, groundnut, pearl millet and sorghum showed detectable biological nitrification inhibition (BNI) in root exudates while among pasture grasses, Brachiaria humidicola (Rendle) Schweick and B. decumbens showed the highest BNI capacity. In another study, Zakir et al. (2008) have reported for the first time the root exuded compound methyl 3-(3-hydroxyphenyl)propionate (MHPP) responsible for BNI by sorghum. Similarly, Subbarao et al. (2013) have reported a root exuded compound, sorgoleone, 1-p-benzoquinone (exuded from sorghum roots) to contribute significantly to the BNI capacity in sorghum.

7.3.1.4 Role of Root Exudates in Nutrient Deficiency The living plant roots produce various organic and inorganic compounds to enhance the adaptation rate of plants to different environmental conditions. The exudation of organic compounds by the plant roots increases with a decrease in soil nutrients. Plants increase their exudation of organic compounds into the rhizosphere under nutrient deficiency. Under Fe deficit conditions, plants exude phytosiderophores into the rhizosphere to adapt to the prevailing condition. Herbaceous or woody plants acquire Fe from the soil by secretion of phytosiderophores that facilitates in acquiring of ferrated-phytosiderophore complexes aided by a highly precise and efficient nutrient uptake system (Römheld 1991; von Wiren et al. 1994, 1995). The rate of root exudation increases is positively related to the tolerance of a plant species to Fe deficiency. Under Fe deficiency, the Fe-deficiency tolerant plant genotypes show more root exudation rates than the plant genotypes sensitive to Fe deficiency (Rengel 2002). The process of phytosiderophore release and its uptake by the plants is solely

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under genetic control (Römheld and Marschner 1990). Several genes are involved in the biosynthesis of phytosiderophores and their precursor nicotianamine that codes for the enzyme nicotianamine synthase (Higuchi et al. 1999). According to the literature, Fe deficiency demands more phytosiderophore production than that under Zn deficiency (Rengel et al. 1998; Walter et al. 1994). This implies to effortless, undeviating and less complicated series of events that are involved in the phytosiderophore triggering process in Fe deficiency than the highly complex triggering process in case of Zn deficiency. Plant genotypes that are tolerant to Zn and Fe deficiency are reported to exude a lesser amount of phytosiderophores than the Zn and Fe sensitive ones in order to increase mobilization of Zn and Fe from sparingly soluble sources (Rengel 2002).

7.3.2

Other Novel Functions of Root Exudates

Root exudates are known to involve in different positive and negative types of interactions that include interactions between plants, plant and soil microorganisms and also between plants, soil microbes and nematodes (tritrophic interactions). Plant -microbe interactions is one of the most common interactions that exist in the rhizosphere microzone which illustrates the tritrophic interactions and the role of root exudates in these interactions. There are a few studies that explained the tritrophic interactions and their occurrence, which is when both the partners the soil microbes and nematodes act synergistically to stimulate growth in plants. A study by Horiuchi et al. (2005) demonstrated that soil-dwelling nematode Caenorhabditis elegans helps in establishing a positive connection between roots and soil rhizobia resulting in healthy and high nodulation in legumes. Briefly, the study elucidated the role of C. elegans in initiating plant-microbe symbiosis. On the release of plant root volatiles, the nematode, C. elegans carry the bacterium to the roots of the legumes resulting in the initiation of plant-microbe symbiosis. Root exudates contain compounds that are known to exert direct influence on shaping the rhizosphere microbial community. The different components in root exudates show positive chemotactic responses in bacteria and the capacity for different microbial species to utilize and compete for substrates (Somers et al. 2004). For example, in one of the reports by Naim (1965), it was documented that the microbial density in the root apex of Libyan desert grass (Aristida coerulescens) was significantly higher than the microbial population found at the base of the plant. A similar pattern was observed for wheat roots (Van Vuurde and Schippers 1980). Looking at the colonizing pattern shown by the microbial communities, it was suggested that this was due to the exudation of certain rhizodeposits predominantly at the root tip. These include root exudates and lysates that is highly predominant at the bases of plant roots. Furthermore, plant roots secrete a wide range of inhibitory substances as secondary metabolites that help the host plants to cope with different bacterial and fungal pathogens in response to inducers that initiate a defence response (Walker et al. 2003). Under natural conditions, plant defence responses remain constantly

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stimulated but exudation of secondary metabolites by plant roots such as saponins, glucosinolates and hydroxamic acids accounts for the resistance or the susceptibility of particular plant species/cultivars to root pathogens. There are several studies that have highlighted the antimicrobial activity exhibited by LMW compounds and the plant defence proteins which are released as a part of plant root exudates. For instance, Lanoue et al. (2010) reported that the barley root system secreted phenolic compounds such as vanillic acid, p-coumaric acid and with antimicrobial activity under Fusarium attack. Similarly, during Pseudomonas aeruginosa infection of basil roots, the basil root system secreted rosmarinic acid that exhibited antibacterial activity against P. aeruginosa under in vitro conditions. Flavonoids were recently reported to show a significant inhibitory effect against different bacterial and fungal plant pathogens. Flavonoids were considered to be an important molecule for conferring resistance to plants against different phytopathogens. The chemiosmotic potential between cytoplasmic matrix and vacuole acts as the primary driving force for the transport of flavonoid molecules to the plant infection site. At the site of infection, the flavonoids induce hypersensitivity reaction and programmed cell death. The antimicrobial activity of flavonoids depends on their ability to inhibit microbial adhesion and the inactivation of cell envelope transport proteins. They can disrupt the microbial membrane, alter membrane permeability and inhibit cell envelope and nucleic acid synthesis by forming hydrogen bonds with the stacking of nucleic acid bases, electron transport chain and ATP synthesis (Mierziak et al. 2014). Additionally, plant roots secrete various proteins to protect the plant against different soil-borne pathogens. For instance, Park et al. (2002) have reported that the roots of the plant Phytolacca americana (pokeweed) are well known for their ability to secrete various plant defence proteins including PAP-H. PAP-H is a ribosomeinactivating protein (RIP) that helps in the inhibition of protein synthesis by acting on the ribosome in a highly specific order. They also exhibit in vitro N-glycosidase activity against fungal ribosomes, whereby they can recognize and depurinate fungal ribosomes. Root exudates have also been shown to alter the genetic make-up of the microbial communities (Baudoin et al. 2003) and enhance the number of pollutant degraders in rhizosphere soil (Joner et al. 2002). Marschner et al. (2002) in one of their studies examined the changes in microbial community profile associated with roots varying in architecture and maturity as a result of variations in root exudation pattern using DGGE analysis. DGGE analysis revealed a prominent difference in microbial communities on the basis of the root type which ultimately affects the compositional content of root exudates. The significant differences in fungal and bacterial community structure were recognized to be the difference in organic acid production by both the communities. For instance, the fungal community is known to produce high concentrations of citric acid, while the bacterial community produces cis-aconitic and malic acid in addition to citric acid. In relation to root exudates stimulating hydrocarbon degrader populations in rhizosphere soil, Cebron et al. (2011) have observed that the major microbial strains in a phenanthrene contaminated soil were Pseudoxanthomonas sp. and Microbacterium sp. before the addition of root exudates, but on the addition of root exudates of ryegrass, the growth of

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Pseudomonas sp. and Arthrobacter sp. were also favoured. This suggests that root exudates have a direct impact on enhancing the microbial diversity of any contaminated piece of land while increasing the abundance of PAH-RHDα gene containing microorganisms for faster remediation of PAH contaminated sites. Secondary plant metabolites, a key component of rhizodeposits, also play a crucial role in plant survival in environments contaminated with different hydrocarbons such as polyvinyl chloride (PVC) and polyaromatic hydrocarbons (PAHs). There are studies reporting that the presence of high concentrations of secondary plant metabolites in the rhizosphere ecosystem enhances the number of pollutant degraders in rhizosphere soil (Donnelly et al. 1994).

7.4

Conclusion and Future Perspectives

The current chapter highlighted a few of the research findings to understand the mechanistic insights of exudation-related plant-microbe interactions as well as rhizosphere functioning. Overall, the chapter provided an illustrated explanation based on the research findings to establish the root exudates as key mediators for successful interaction between plants and rhizosphere microbes in the rhizosphere microzone. But due to a bottleneck in a comprehensive understanding of root exudates chemistry, there is a lack of information and knowledge about belowground plant-microbe interactions. Although several components of root exudates have been characterized, studied and explained in detail, the metabolic profiling of the root exudates has not been explored in detail except for a few components such as organic acids, flavonoids and fatty acids. This can be majorly due to the inadequacy and limitation of technology to isolate and characterize the minute portions of the natural products that are highly alterable in nature. Moreover, experimental works corresponding to spatiotemporal pattern study of root exudates are mostly under axenic or monoxenic laboratory conditions and thus require more attention for conducting in-planta studies to understand the mechanistic insights of root exudates in belowground plant-microbe interactions as well as their dynamic role in plant growth and development. Although much is known in regard to the role of root exudates in an interactive activity, a still more is required to have a good understanding of the exudation pattern of different plant roots belonging to different species, the variations in exudation with respect to plant age, soil type, environmental parameters and rhizosphere microbiome. Furthermore, the fate of root exudates in rhizosphere soil and the function of these exuded materials in microbial physiology and functions have not been explored in detail. Thus there is a huge scope for researchers to undertake metabolomic studies to improve the understanding and knowledge of the same. Moreover, it opens up several opportunities for the researchers to take up studies to understand the interlink between bacterial gene expression and the nature of exuded material from the living plant roots.

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Rhizospheric Microbial Diversity: Organic Versus Inorganic Farming Systems Asha Sahu, Asit Mandal, Anita Tilwari, Nisha Sahu, Poonam Sharma, and Namrata Pal

Abstract

The agricultural system is very much dependent on the interaction and association of plants with the rhizospheric soil microbes. The microbial diversity found in the rhizosphere is unique and distinct from the other parts of the soil. The rhizospheric population is very important in terms of plant nutrients. Field studies reveal that different farming practices, namely, organic and inorganic farming systems, decide the soil microbial population and diversity, but information on the effect of these systems on the rhizospheric group is meagre. This chapter is an attempt to review the effects of organic and inorganic systems on rhizospheric plant-soil-microbe interactions.

A. Sahu (*) · A. Mandal · N. Sahu ICAR-Indian Institute of Soil Science, Bhopal, Madhya Pradesh, India e-mail: [email protected] A. Tilwari Madhya Pradesh Council of Science and Technology, Bhopal, Madhya Pradesh, India P. Sharma ICAR-Indian Institute of Soil Science, Bhopal, Madhya Pradesh, India ICMR-National Institute for Research in Environmental Health, Bhauri, Bhopal, Madhya Pradesh, India N. Pal ICMR-National Institute for Research in Environmental Health, Bhauri, Bhopal, Madhya Pradesh, India # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2022 U. B. Singh et al. (eds.), Re-visiting the Rhizosphere Eco-system for Agricultural Sustainability, Rhizosphere Biology, https://doi.org/10.1007/978-981-19-4101-6_8

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8.1

Introduction

8.1.1

Plant-Microbe Relationship and Rhizosphere

Overexploitation of the soil for more crop production to feed the ever-increasing population has led to the deterioration of soil quality and its health. The capacity or potential of soil in terms of crop productivity and soil fertility defines soil quality or soil health (Williamson et al. 2011). Agricultural ecosystems will be resilient, resistant and redundant only when the health of the soil is good, and thus soil health or quality is redefined as the capacity of soil in terms of living organisms (Karlen et al. 2003), becoming also increasingly relevant as soil ecosystem services (Garbisu and Epelde 2011). The most important and critical point is to find out the indicators for sustainable agriculture which are associated with effective nutrient cycling (Rooney et al. 2009), particularly mediated by soil microbiological activities, its diversity and functionality (Babalola et al. 2007; Allison and Martiny 2008). Thus, the soil microbial biomass/communities are conceded as very important indicators as well as regulators of agroecosystems. It is a fact that these regulators and their spatial and temporal functions depend on the type of agricultural practices or systems (Hartman et al. 2018). Effects of different soil management systems, namely, organic system (where no synthetic inputs are provided) versus inorganic systems, showed diversified soil properties and microbial communities (Azevedo Jr. et al. 2017). Also, long-term field experiment studies revealed contrasting effects of different agroecosystems on physicochemical properties of soil (Crittenden and de Goede 2016), microbial biomass (Amaral et al. 2011) and habitat-specific bacterial and fungal taxa (Chen et al. 2018). Contextual variables in an agroecosystem such as soil type, climate and cropping system mostly influence the soil properties at a spatial scale. Dependency on chemical fertilizers is more than the application of organic manure in a conventional inorganic system although excessive use of chemical fertilizers affects soil quality, reduces nutrient uptake by the crop and increases environmental hazards such as greenhouse emissions and eutrophication (Zhu et al. 2016). With the need to achieve sustainability in agriculture and to address the environmental concerns adhered with the use of chemical fertilizers, researchers are finding out a way to either substitute chemical inputs with inorganic or promote the balanced/integrated nutrient system by combining both the inputs (Bhattacharyya et al. 2008). It was proved in the recent past that irrespective of climatic conditions and experimental sites, the microbial diversity and the functionality were more in the organic system because of the nutrient enrichment of the soil (Hamm et al. 2016). Owing to the improved soil carbon and nitrogen, an enhanced population of certain bacterial strains was observed in the compost (organic manure) applied field (Chaudhry et al. 2012). Nevertheless, plants also regulate rhizospheric microbial communities either through rhizodeposition or by moisture and temperature control (Denef et al. 2009). Thus, it can be concluded that microbes play a vital role in the biogeochemical cycling processes in the soil and also the bulk soil communities

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Fig. 8.1 Rhizospheric soil with plant-microbe interaction (https://www.slideshare.net/ ashwincheke/plant-microbe-interaction-by-dr-ashwin-cheke)

affect the unique environment of rhizospheric microbial communities (Zhang et al. 2018; York et al. 2016). The soil rhizosphere is known as a hotspot where dynamic relationship and interaction occurs between plant roots and microbial communities present in the soil (Fig. 8.1). The plant roots release exudates in the form of organic acids, amino acids and sugars to attract microbes, which in turn release antimicrobial compounds to protect plants against pathogens. These allow the microbes such as fungi and bacteria to cause the breakdown of the organic matter and thus help in nutrient release and cycling (Kuzyakov 2002), promoting plant growth directly or indirectly (Lugtenberg and Kamilova 2009) and suppressing plant pathogens (Hayat et al. 2010). If we see the agricultural system management from ecosystem services or nutrient flux point, it becomes necessary to analyze soil processes and soil properties to understand the complex relationship between management systems, particularly focused on the rhizosphere (Ryan et al. 2009; Luo et al. 2018). But the unique mechanisms of rhizospheric microbes (Guo et al. 2018) are likely linked to the performance of the plants (Rout and Southworth 2013). Since the rhizospheric soil is controlled by the plant and soil microbial processes, it is very difficult to predict the functional implications of rhizospheric communities.

8.1.2

Rhizosphere Exudates and Nutrient Availability

The rhizosphere is called the interface of root and soil, where the soil is influenced by plant roots. The rhizosphere is characterized by the prevalence of greater microbial activity than the non-rhizosphere or soil away from the roots of the plants. The term ‘rhizospheric effect’ indicates the overall influence of plant roots on soil

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microorganisms which include species of bacteria, fungi, actinomycetes and other organisms such as nematodes, protozoa and algae. The rhizosphere effect is due to the rhizodeposits from the roots, which attract some microorganisms. In the rhizosphere, about 50% of the photosynthates are transferred into the roots, only about 1% are actively released as root exudates and 10% are lost as root debris (Uren 2007). Rhizodeposits/exudates include a variety of substances that originate from sloughed-off root cells and tissues, mucilages, volatiles, soluble lysates and exudates that are released from damaged and intact cells (Dakora and Phillips 2002). Root exudates comprise the largest fraction of non-volatile rhizodeposits (Meharg and Killham 1988) and are complex mixtures of low molecular weight organic compounds including carbohydrates, amino acids, organic acids, phenolics, fatty acids, sterols, vitamins, enzymes, purines/nucleosides as well as inorganic ions (HCO3 , H+) and gaseous molecules (i.e. CO2, H2) (Dakora and Phillips 2002) (Table 8.1). Among these components, organic acids, amino acids and carbohydrates are generally released in the largest quantities (Farrar et al. 2003).

8.2

Microbial Diversity in Different Land Systems

Microorganisms play an important role in many ecosystem services and also provide support to all living forms. The land system has complex and huge microbial biodiversity, which plays important role in the management of natural habitats (Table 8.2).

8.3

Inorganic Versus Organic Microbial Shifting

Microbes are the key drivers in maintaining the functionality of the agroecosystem. It is also important to study the impact of the different farming practices on the microbial population or communities in the soil. Shifting the conventional inorganic farming practices to organic practices has also shifted the microbial communities of the system towards a positive organization for a sustainable ecosystem. A number of studies suggest that microbial abundance and diversity were more in soil under organic management system as compared to the soil under conventional (inorganic) practice. This upsurge in microbial diversity could be associated with reduced tillage, cover cropping and usage of organic fertilizers. As a result of this, soil organic carbon increases and serves as an energy source for heterotrophic microbiota (Liao et al. 2018). If organic farming practices have been applied for long term, it can be assumed that the soil microbial composition has shifted and improved the turnover of the soil organic matter. The relative abundance of microbes varies with the system as shown in Fig. 8.2 and Table 8.3. The shifting of the microbial community is owed to the change in the nutrient content of the soil, especially for the increased salinity and accumulated nutrients. An example of different farm practices can be seen in the shifting of iron redox bacterial communities that influence the iron cycle in the soil. The soil that is

Nonproteinogenic amino acids, for example, mugineic acid and its derivatives

Amylase, invertase, phosphatase or phosphohydrolase, protease, polygalacturonase

Phytosiderophore

Enzyme

Carboxylic acids or organic acid

Amino acid and amide

C and N source for microorganisms P mobilization by maleic, citric, tartaric acid P acquisition Mobilization of P, Fe, Mn and Zn in the soil (chelation and reduction) Increases P availability by carboxylates Detoxification of Al3+ (chelate and complexation) K mobilization by organic acids Mobilization of trace elements, for example, Fe (barley > wheat > oat > rye > corn > sorghum > rice) Mobilization of Zn, Cu and Mn is reported due to rhizosphere acidification Amylase helps in N mineralization Invertase enhances C mineralization Protease plays a role in N mineralization Phosphatase- P solubilization (acid phosphatases and phytases) Polygalactoturase- N mineralization

The C and N present in amino acid and amide easily be taken up by microorganisms Increases N availability in soil

(continued)

Das and Varma (2010), Song et al. (2020), Das and Varma (2010), Tarafdar and Marschner (1994), Neumann and Romheld (2001), Arshad Jr and Frankenberger (1998)

Neumann and Romheld (2001)

Jones (1998), Wang and Lambers (2020), Nadira et al. (2016), Shane and Lambers (2005), Ryan et al. (2014), Dinkelaker et al. (1993), Neumann and Romheld (2001)

Moe (2013), Gent and Forde (2017), Phillips et al. (2004)

Root exudates Sugar

References Gunina and Kuzyakov (2015), Ratnayake et al. (2013), Gransee (2001)

Table 8.1 Different root exudates and their function in nutrient availability in soil Functions in nutrient availability Sugar serves as C and N source for microorganisms Greater effect on P mobilization in soil

Rhizospheric Microbial Diversity: Organic Versus Inorganic Farming Systems

Substances identified Arabinose, fructose, fucose, galactose, glucose, maltose, oligosaccharide, raffinose, rhamnose, ribose, sucrose, xylose Asparagine, aspartic acid, α-alanine, β-alanine, arginine, cystine/cysteine, glutamine, glycine, histidine, lysine, methionine, phenylalanine, proline, serine/homoserine Acetic, butyric, citric, glutaric, lactic, maleic, malic, malonic, oxalic, propionic, pyruvic, succinic, tartaric, valeric

8 157

Others

Phenolic acid and coumarin

Root exudates Growth factor

Substances identified p-Amino benzoic acid, auxins, biotin, choline, inositol, n-methyl nicotinic acid, niacin, pantothenate, pyridoxine, thiamine Coumarin, cinnamic acid, caffeic acid, ferulic acid, salicylic acid, syringic acid, vanillic acid Flavanone, fatty acids, proteins, sterols, lipids, aliphatics, aromatics, vitamins, carbohydrates

Table 8.1 (continued)

Riboflavin enhances Fe acquisition Aliphatic and aromatic organic acids, vitamins and carbohydrates moderate trace metal toxicity Soil carbohydrates for rhizobium improve N fixation

Mobilization of Fe and Mn and Fe mobility Detoxification of Al3+

Functions in nutrient availability Increase nutrient availability (N, P), micronutrient solubilization

Clemens and Weber (2016), Römheld (1987), Dakora and Phillips (2002) Chen et al. (2017), Vranova et al. (2013), Abd-Alla et al. (2014)

References

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Table 8.2 Different microbial diversity in different land systems Land system/ landscape Forest soils

Pine forest soils

Deciduous forests Acidic soils of coniferous forests Agriculture soils

Landfills

Rhizosphere

Litter and deadwood

Grasslands

Shrubland

Types of microorganisms Alpha- and Delta proteobacteria, Actinobacteria and Acidobacteria Proteobacteria (Burkholderiales, Caulobacteriales, Rhizobiales and Xanthomonadales), Bacteroidetes (Sphingobacteriales) and Acidobacteria Proteobacteria, Actinobacteria, Bacteroidetes and Acidobacteria Alpha Proteobacteria, Acidobacteria and Actinobacteria Proteobacteria, Acidobacteria, Actinobacteria, Gemmatimonadetes, Firmicutes and Verrucomicrobia, Bacteroidetes, Microvirga, Nocardioides, Oligotrophic taxa, Chlorofexi, mineral weathering bacteria and bacteria associated with ECM fungi Epsilon proteobacteria, Gamma proteobacteria, Clostridia and candidate division OP3 Actinomycetes Bacillus, Paenibacillus, Pseudomonas, methanotrophic bacteria, ammonia-oxidizing bacteria, and N2-fixing bacteria, Clostridium spp., Arthrobacter spp., Brevibacterium spp., Corynebacterium spp., Serratia, Enterobacter and Rhizobium spp. Acinetobacter, Agrobacterium (α-Proteobacteria), Alcaligenes (β-Proteobacteria) and Xanthomonas (γ-Proteobacteria). Acidobacterium, Bacteriodetes, copiotrophic bacterial strains and ECM Fungi Proteobacteria and Bacteriodetes, Cellulolytic taxa and fungal mycelia degraders, Nitrogenfixing Bacteria, litter and dead wood decomposing bacteria (Burkholderia, Phenylobacterium and Methylovirgula) and fungi Chitinophaga, Ewingella, Pseudomonas, Pedobacter, Variovorax, Stenotrophomonas genera that are known to produce chitinolytic enzymes Imperata cylindrica, Microstegium fasciculatum and Murdannia triquetra. Lotus wrangelianus, Hemizoniacongesta, Holocarpha virgata, Plantago erecta and Lasthenia californica Pyracantha fortuneana, Vitex negundo and Alchorneatrewioides

Reference Min Song et al. (2018), Lladó et al. (2017), Uroz et al. (2013) Lladó et al. (2017)

López-Mondéjar et al. (2015) Lladó et al. (2017)

Lauber et al. (2009)

Blake et al. (2016)

Garbeva et al. (2004), Latif et al. (2020)

Brabcová et al. (2016), Kielak et al. (2016)

Batten et al. (2006)

Batten et al. (2006)

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8%

10%

20%

Bacteria

0

Eukaryota

a 30%

Virus

40%

b

Archaea

Bacteria Eukaryota

18%

Virus Archaea

21%

Fig. 8.2 Relative abundance of microbes in percentage. (a) Organic system. (b) Inorganic system

maintained under inorganic fertilization shows a higher abundance of ferric (Fe3+) reducing bacteria (e.g. Geobacter), while the soil under organic fertilization regimes shows a higher amount of Pseudomonas and Anaerolinea, which are Fe2+ oxidizers (Wen et al. 2018). In addition to this, Nakhro and Dkhar’s findings (2010) revealed that organic carbon inputs showed a significant positive correlation with fungal and bacterial populations as organic farming practices elevated the carbon content, thereby increasing the microbial counts in the soil. The soil under conventional practice had a low organic carbon content that affected the microbial population. It was observed that members of the phyla Bacteroidetes and Planctomycetes were more abundant under organic management, whereas members of the Actinobacteria and Verrucomicrobia tended to be more abundant in the soil under conventional practices (Fernandez et al. 2020). Luo et al. (2017) had performed a research on the agri-soil and shown the increased ratios of fungi to bacteria (F/B), Gram-positive to Gram-negative (G+/ G ) and arbuscular mycorrhizal fungi (AMF) to saprotrophic fungi (AMF/SF) upon increased manure input for 8 years. This suggested that certain microbial groups, such as G+ bacteria, fungi and AMF, are more adapting to organic farming than the other ones. It has also been observed that the application of the organic manures accelerates the aggregation of the soil, that is, the formation of macroaggregates increases the organic carbon concentration in the aggregates than the conventional inorganic NPK fertilizer. These aggregates provide more suitable microhabitats for anaerobic microbes (Zhang et al. 2014). Applying organic manures or organic farm practices not only increase the biomass of individual microbial group but also alter their community structure. When the native microbes utilize the exogenous supply of the organic carbon source, it leads to a change in community composition; that is, as soon the organic compounds are added to the soil, the fast-growing Gram negative bacteria start proliferating. After a while, their population decreases allowing the growth of other groups such as Gram positive bacteria and fungi (Lazcano et al. 2013). Also, as we discussed above, organic inputs may accelerate the soil aggregation, generating pores larger in size. This facilitates the fungal growth and explains better the higher number of fungus and actinomycetes (G+ bacteria) in organically managed soils (Strickland & Rousk

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Table 8.3 Relative abundance of microbes in the organic and inorganic systems Relatively abundant microbes in an organic system Bacteria: Bacillus (Firmicutes), Butyrivibrio (Firmicutes), Glycomyces (Actinobacteria), Leptolyngbya (Cyanobacteria), Microbulbifer (Proteobacteria), Methylocaldum (Proteobacteria), Nostoc (Cyanobacteria), Planctomyces, Pseudoxanthomonas (Proteobacteria), Roseiflexus Bacteria: Alpha-Proteobacteria, Gammaproteobacteria, Firmicutes, Rhodobium Fungi: Mortierella, Verticillium Bacteria: Actinobacteria and Nitrospirae Viral families: Circoviridae, Inoviridae, Microviridae Bacteria: Korarchaeta, Eukaryarchaeota, Saccharomonospora, Sorangium Bacteria: Pseudomonas, Anaerolinea, Aquincola, Clostridiales, Dechloromonas Bacteria: Desulfuromonadales, Clostridiales, Erysipelotrichales, Rhodocyclales and Rhodobacterales Fungi: Glomeromycetes (unclassified class), Cantharellales, Saccharomycetales, Trichosporonales, Agaricales and Onygenales Protist: ThraustochytridaThecamoebida, Labyrinthula and Heterolobosea

Relatively abundant microbes in the inorganic system Bacteria: The genera Rhodoplanes (Proteobacteria) and Skermanella (Proteobacteria), Archeal phylum Crenarchaeota and the genus Candidatus Nitrososphaera

Bacteria: Actinobacteria, Chloroflexi, Acidobacteria, Nitrospirae, Nocardioides, Marmicola Fungi: Ascomycota, Alternaria, Davidiella Dothideomycetes, Leotiomycetes Bacteria: Proteobacteria and Fibrobacteres Viral families: Myoviridae, Podoviridae, Siphoviridae Bacteria: Nanoarchaeota, Crenarchaeota, Firmicutes, Thaumarchaeota, Nocardiodes Bacteria: Geobacter, Clostridium, Desulfosporosinus, Desulfitobacter, Peptocaccaceae, Desulfurispora, Bateroidales Bacteria: Bacillales, Deinococcales, Micrococcales, Acidobacteriales, Kineosporiales and Streptomycetales Fungi: Paraglomerales, Eurotiales, Neocallimastigales and Chaetothyriales Protist: Prasiolales, Tribonematales, Cryptofilida, Phytiales, Dermamoebida and Bicoecales

References Liao et al. (2018)

Francioli et al. (2016)

Ai et al. (2015) Enebe and Babalola (2020)

Wen et al. (2018)

Harkes et al. (2019)

2010). Such microbial groups accumulate more SOC, proving better for the soil fertility and biological quality (Luan et al. 2020). From soils under organic farming at different locations, the average microbial population of fungi, bacteria and actinomycetes was recorded as 56.9%, 55.2% and 49.5%, respectively, which was

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comparatively higher than those in the conventionally managed soils (Sheoran et al. 2018). Moreover, a study showed that in some cases the same genera can be prevalent in both conventionally and organically managed soils with limited differences. Some microbial groups showed highly reliable differences on the account of statistics among Bacillus and Gemmatimonas, which were more prevalent under conventional practice; also, among the genera with the higher count in organically managed soil, namely, Holophaga, Acidobacteriaceae, Hyphomicrobium, Flavobacterium and Nocardioides ( p < 0.05). They also studied the relative abundance of the phylum Actinobacteria in the organic wheat soil, finding the lower taxa contributing utmost to the change. With a relative abundance of more than 1%, the orders of Actibacteria-Rubrobacter, Acidimicrobium and Solirubrobacterales constituted 5.83% in soil under organic farming, that is, twice of those in the conventional soil system (Armalytė et al. 2019). Thus, it can be concluded that the organic system exerts positive and beneficial effects on soil biological properties, particularly microbial community, diversities, heterogeneity and richness. Nevertheless, the response of farming systems to rhizospheric microbial communities is very complex and magnificent.

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Rhizomicrobes: The Underground Life for Sustainable Agriculture Tanwi Sharma, Manoj K. Dhar, and Sanjana Kaul

Abstract

Sustainable agriculture can be considered the first step towards a sustainable world. Besides other human activities, agriculture is one of the root causes of the introduction of harmful chemicals into the environment. Therefore, one cannot imagine the existence of a sustainable world without realizing the existence of sustainable agriculture. Sustainable agriculture is the integration of efforts towards achieving socio-economic equality, economic growth and environmental preservation. Harnessing the plant beneficial microbes in agriculture for minimizing the use of non-biodegradable chemicals is a progressive endeavour towards sustainable agriculture. Plant microbiomes are emerging as promising niches to be explored for plant beneficial microbes. Plant microbiomes harbour endophytes, epiphytes and rhizomicrobes as well. In this chapter, we will discuss the possibilities of harnessing rhizomicrobes in the field. Microbes associated with the rhizosphere of the host plant are known as Rhizomicrobes. Rhizomicrobes are known to bestow their host plant with numerous plant growth promotion properties such as Biocontrol, Biofertilization, Phytostimulation, Rhizoremediation, Stress resistance and many more. Rhizomicrobes contribute not only to plant health but also to the improvement of soil fertility. A deep understanding of the role and reality of rhizomicrobiomes of different plants is the need of the hour as such microbes can be successfully harnessed in agriculture as biofertilizers in place of chemical fertilizers. Therefore, rhizomicrobes can play an important role in transforming the present agriculture system into the sustainable one.

T. Sharma · M. K. Dhar · S. Kaul (*) School of Biotechnology, University of Jammu, Jammu, Jammu and Kashmir, India # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2022 U. B. Singh et al. (eds.), Re-visiting the Rhizosphere Eco-system for Agricultural Sustainability, Rhizosphere Biology, https://doi.org/10.1007/978-981-19-4101-6_9

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Introduction

Continuous use of chemical fertilizers in the agriculture system is not only polluting the environment but also posing threats to human health (Gupta et al. 2015). Application of green manures and biofertilizers is the need of the hour to save the environment as well as life on the earth. Plant microbiome studies can prove to be helpful in the isolation and selection of plant beneficial microbes to be used as green manures/biofertilizers. Plants are known to be associated with complex microbial communities. Such complex microbial communities constitute the holomicrobiome of the host plant. Broadly, the holomicrobiome of a plant can be differentiated into three compartments, namely, phyllosphere, endosphere and rhizosphere. The phyllosphere of a plant is harboured by epiphytes, the endosphere by endophytes and the rhizosphere by rhizomicrobes. These microbes may be associated with the host plant through symbiotic, mutualistic or pathogenic interactions. The rhizosphere and its associated microbes together constitute Rhizomicrobiome. Based on the interactions with the host plants, rhizomicrobes can be differentiated as symbiotic rhizomicrobes and free-living rhizomicrobes. Root exudates of the host plant influence the composition of microbial communities associated with the rhizosphere (Hartmann et al. 2008). Morgan et al. (2001) have defined the phenomenon of attraction of active soil microbial communities towards roots exudates as the Rhizospheric effect. The rhizosphere is richer in nutrients as compared to the bulk soil. Therefore, in the rhizospheric zone of a plant, there are 10–100 times more microbes as compared to that present in the bulk soil. The rhizosphere is found to be inhabited by fungi, bacteria, archaea, protozoa, algae, viruses, oomycetes, microarthropods and nematodes. Bacteria and fungi are the prominent microbial groups among rhizospheric microbiota but rhizospheric fungi are less explored microbiota colonizing the rhizosphere as compared to the rhizospheric bacteria (Pattnaik and Busi 2019). Rhizomicrobes act as plant growth promoters directly or indirectly by synthesizing growth regulators, antibiotics, lytic enzymes, siderophores and nitrogen fixation etc. In the direct mechanism, they promote plant growth via biofertilization, rhizoremediation, root growth stimulation and stress tolerance. In the indirect mechanism, they act via antibiosis, posing competition for nutrients and niches, inducing systemic resistance. Having the vision of sustainable agriculture, advanced crops are expected to be resistant/tolerant of different diseases and stress conditions. Plant growth promoting rhizomicrobes can thus be successfully used as biofertilizers to achieve agricultural sustainability (Fig. 9.1).

9.2

Modern Techniques to Explore Rhizomicrobes

Rhizomicrobes are known to bestow their host plant with numerous plant growth promotion properties such as Biocontrol, Biofertilization, Phytostimulation, Rhizoremediation and Stress resistance. Deep and detailed studies of rhizomicrobes can prove to be helpful to plan the strategies for crop improvement using

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Fig. 9.1 Unsustainable versus sustainable agriculture

rhizomicrobes for sustainable agriculture. The application of modern tools and techniques in the field can give us a closer view of the interactions among the different rhizomicrobes as well as with the host plant. Modern Omics and Metaomics techniques can be successfully used to study the rhizospheric microbial communities in terms of their composition and colonization, diversity and distribution and their associations and interactions (Fig. 9.2) (Pascual et al. 2016; Baeshen 2017). Metagenomic studies of the plant rhizospheres can prove to be helpful in unravelling the metabolic potential and other plant beneficial attributes of the rhizomicrobes without even culturing them. The comparative metagenomics technique can be used to study the functional diversity among the rhizomicrobiomes of different plants or the same plant under different environmental conditions. Advanced Next-generation sequencing technology has made metagenomic studies comparatively easier. Transcriptomic and metatranscriptomic studies can reveal the differential expression of genes among symbiotic and free-living rhizomicrobes. Comparative transcriptomic studies can prove to be helpful in finding the differential gene expressions in the same microbial species residing in the rhizosphere and bulk soil or some other habitat. Such information is needed for realizing the use of PGPR (plant growth promoting rhizobacteria) in agriculture as biofertilizers. Further, proteomic and metaproteomic studies of the rhizospheres are helpful in determining the actual functional roles of the rhizomicrobes in the plant health and productivity. The mass spectroscopy technique has made proteomic studies comparatively easier. Metaproteogenomic studies link the genomic and proteomic studies and the data so obtained can prove to be helpful in determining the actual potential of the microbes

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Fig. 9.2 Techniques to study different aspects of rhizomicrobiome

for sustainable agriculture. Besides using classical tools such as Microscopy counts, Phospholipid fatty acid analysis (PLFA), Fatty acid methylated esters analysis (FAME) and DNA fingerprinting, modern tools such as Microarray, next-generation sequencing (NGS), pyrosequencing, stable isotope probing (SIP), fluorescence in situ hybridization (FISH) and metabarcoding can also be successfully used for quick and detailed analysis of the rhizomicrobiomes (Abdelfattah et al. 2018). Therefore, multidisciplinary studies are needed to be done in the field of rhizomicrobiome for a better understanding of the niche as a whole so that the actual potential of the rhizomicrobes can be harnessed in a more efficient and sustainable way.

9.3

Techniques to Introduce PGP Microbes in Agriculture

Owing to their plant beneficial attributes, the introduction of rhizomicrobes in agriculture will lead to increased agronomic efficiency in a sustainable way. Successful microbial inoculation in the target host plant is the first step towards the colonization and plant-microbe interactions. The introduction of microbes to the target host cell is termed bioinoculation and the microbes used are termed bioinoculants. Plant growth promoting rhizomicrobes can be used as bioinoculants in plants, seeds, roots and soil (Bashan et al. 2014). Successful bioinoculation of

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selected potential rhizomicrobes in crops would result in phytopathogen-resistant plants with improved plant growth and productivity (Parasuraman et al. 2020). Liquid inoculation and nano-encapsulation techniques can prove to be helpful in realizing the use of plant growth promoting microbes as biofertilizers. de Oliveira et al. (2018) have successfully used the liquid inoculation method to inoculate Azospirillum lipoferum in Myracrodruon urundeuva seeds. The inoculated plants have been found to be more tolerant to drought stress. Conversely, Montiel et al. (2017) have found the microencapsulation method to be more efficient as compared to the liquid inoculation method. It has been observed that alginate microencapsulation-based immobilization of P. putida, associated with the tomato rhizosphere, results in improved growth and productivity in tomato plants (Montiel et al. 2017). Microencapsulation method based inoculation is preferred for improved microbial adhesion, microbial colonization of root cells and permanency. The success of the inoculation method is assessed in terms of the plant response. The response of plants to the microbe inoculation is affected by different factors, such as inoculation method, environmental conditions, inoculant species, inoculant density and soil type. Also, multistrain bioinoculants are found to be more potent in terms of plant growth promotion as compared to monostrain-bioinoculants. Bioinoculants supplemented with nanocompounds are also found to be more effective. Chaudhary et al. (2021) have studied the combined effect of nanocompounds and PGPR bioinoculants on the growth and yield of Zea mays plants. The study revealed that the combined treatment of nano-zeolites and PGP Bacillus-based bioinoculants to the maize plant leads to improved plant growth in terms of weight and length of roots and shoots as well as carotenoids, chlorophyll, proteins, carbohydrates and phenol content in the inoculated plant as compared to the control. Pereira et al. (2010) have studied the effects of the size of bioinocula on the inoculated plants. The study has revealed that bio-inoculum with a high concentration of multiple PGPR is more effective towards improved plant growth under drought stress. Therefore, keeping eye on the impacts of all the studied factors, new efficient methods of bioinoculation need to be explored for the successful harnessing of rhizomicrobes towards sustainable agriculture.

9.4

Importance of Rhizomicrobes

Rhizomicrobes are well-known plant growth promoters bestowing the host plant with improved health and yield. Besides their importance in the agriculture sector, rhizomicrobes also find applications in the field of Biomedicine, textile and food processing industries and many more for environmental sustainability (Pattnaik and Busi 2019), but in the present chapter, we will discuss the importance of rhizomicrobes towards the achievement of agriculture sustainability. Rhizomicrobes lead to plant growth promotion in three different modes, namely, Biofertilization, Biostimulation and Biocontrol (Fig. 9.3). Biofertilization involves facilitating the assimilation of soil nutrients, Biostimulation involves the synthesis of

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Fig. 9.3 Benefits of rhizomicrobes

phytostimulating hormones and Biocontrol involves the suppression of plant diseases.

9.4.1

Biofertilization

Indiscriminate use of chemical fertilizers is leading to a continuous drop in the Nutrient use efficiency (NUE) in crops, which is posing a serious threat to future food security. Owing to the non-availability of the complex and insoluble soil nutrients to the plants for direct use, the chemical fertilizers appear as the easy alternatives to meet the nutrient demands of the crop plants. As a result, there is a continuous accumulation of harmful chemicals in the environment. Therefore, there is a need to find out some eco-friendly alternatives to meet the nutrient supply of crops. Rhizomicrobes are known to solubilize complex soil nutrients into simple and soluble forms for the direct use of host plants. Biofertilization seems to be one of the characteristics of the rhizomicrobes which can be harnessed to fulfil nutrient demands of the crop plants in a more sustainable way. Biofertilization includes phosphate solubilization, siderophore production and nitrogen fixation potentials of the rhizomicrobes.

9.4.1.1 Phosphate Solubilization Rhizomicrobes are not only beneficial to the host plant but also contribute to enhancing the fertility of the soil. The soil improvement and plant growth promotion characteristics of the rhizomicrobes are the result of their ability to solubilize, mineralize and decompose available nutrients (Satyaprakash et al. 2017). Phosphorus is one of the essential nutrients needed for the proper growth and development of

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plants. Phosphorus is present in the soil but in a complex insoluble form, which is difficult for the plants to absorb. As a result, artificial Phosphorus fertilizers are used to meet the crop demands, which leads to heavy metal accumulation in the soil. Therefore, eco-friendly alternatives are needed to be searched to avoid the adverse effects of chemical fertilizers on the environment. Interestingly, rhizomicrobes are reported as potential phosphate solubilizers (Gupta et al. 2015). They play an important role in P cycling. Rhizomicrobes are found to follow two types of mechanisms to solubilize phosphorus (Wang et al. 2017). One mechanism includes the secretion of phosphate solubilizing enzymes like phosphatases and the second mechanism includes the production and release of organic acids such as citric acid, acetic acid, lactic acid, succinic acid and malic acid by the rhizomicrobes to solubilize phosphorus. The efficiency or amount of phosphate solubilization is found to be affected by the microbial strain, type of organic acid produced, type of C source used and the type of phosphate to be solubilized (Marra and de Oliveira-Longatti 2019). Various studies are available regarding the P solubilizing ability of rhizosphereassociated bacteria as well as fungi. More specifically, Rhizobacteria are found to be more efficient P solubilizers as compared to their fungal counterparts (Satyaprakash et al. 2017). Different rhizobacterial genera, namely, Pseudomonas, Rhizobium, Bacillus, Arthrobacter, Serratia, Enterobacter and many more, are reported as potential phosphate solubilizers (Gupta et al. 2015; Chauhan et al. 2017), whereas Aspergillus, Penicillium and Fusarium are reported as potential phosphate solubilizing fungal genera (Elias et al. 2016). Singh et al. (2020) have isolated 18 bacterial strains from the rhizosphere of sugarcane plants with phosphate solubilization potential. The fungi associated with the rhizosphere of Arabis alpina have been found to improve plant growth and P uptake in P-poor soil (Almario et al. 2017). Therefore, the use of phosphate solubilizing rhizomicrobes in the soil as biofertilizers can prove to be an eco-friendly and sustainable alternative to the chemical (P) fertilizers.

9.4.1.2 Nitrogen Fixation Nitrogen is the most essential plant macronutrient. Atmospheric nitrogen cannot be directly used by plants. Therefore, chemical nitrogen fertilizers generally in the form of urea are used to meet the nitrogen demands of the crops. This, in turn, results in acidification of soil as well as water and also causes air pollution. Hence, there is a need to find sustainable nitrogen source alternatives for the crops. The plant growth promoting rhizomicrobes with nitrogen-fixing potential can be considered a reliable nitrogen source for sustainable crop production while maintaining the fertility of the soil. Nitrogen-fixing microbes use a nitrogenase enzyme system to fix atmospheric nitrogen which is otherwise unavailable to the plants for direct use (Gaby and Buckley 2012). The efficiency of nitrogen fixation is mainly influenced by the type of soil and soil conditions, nitrogen-fixing microbial strain, plant species and so on (Singh et al. 2020). The rhizobacterial genera such as Azotobacter, Azospirillum, Bacillus, Burkholderia, Cyanobacteria, Enterobacter, Pseudomonas and Diazotrophicus are reported as potential nitrogen fixers for the host plants (Bhattacharyya and Jha 2012; Singh et al. 2020). Singh et al. (2020) have isolated

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22 bacterial strains from the sugarcane rhizosphere with nitrogen-fixing potential. They have studied the nitrogen fixation in sugarcane plants inoculated with B. megaterium and B. mycoides strains. Therefore, nitrogen-fixing Bacillus species associated with rhizospheres can be successfully used as biofertilizers. The significance of studying the nitrogen-fixing rhizomicrobes lies in the fact that the biological nitrogen-fixing ability of such microbes can be extended to non-leguminous plants also. There is a need to isolate and identify PGPR associated with different crops that can perform potentially under different environmental conditions.

9.4.1.3 Siderophore Production Iron is also one of the essential nutrients for plant growth and development, but it is not present freely in the environment for plant use. Plant-associated microbes play an important role in iron assimilation by the host plants. Such microbes produce low molecular weight, iron chelating agents known as siderophores (Winkelmann 2007). Siderophores produced by plant growth promoting rhizomicrobes mostly belong to the carboxylate, hydroxamate and catecholate families (Beneduzi et al. 2012). Siderophore production potential of rhizomicrobes results in both direct and indirect growth promotion of host plants. In the direct plant growth promotion mechanism, rhizomicrobes synthesize siderophores for improved iron assimilation for the host plant. Enhancement in the overall uptake of iron by host plants results in improved plant growth and yield. In the case of indirect plant growth promotion mechanism, rhizomicrobes produce iron sequestering siderophores to create an iron-deficient environment for the pathogenic microbes sharing the same niche. In this way, rhizomicrobes promote the growth and yield of host plants in an indirect way by restricting the proliferation of pathogenic microbes. Bacillus, Azotobacter, Burkholderia, Pseudomonas, Serratia, Rhizobium and Streptomyces are the wellknown rhizobacterial genera with siderophore production potential (Gupta et al. 2015). Various rhizospheric Pseudomonas species, namely, P. fluorescens, P. putida and P. syringae, are reported to possess biocontrol potential against phytopathogens via siderophore production (Shanmugaiah et al. 2015). Patil et al. (2014) have reported siderophore producing rhizospheric B. subtilis species with biocontrol potential against phytopathogenic fungi. Siderophore producing rhizomicrobes are also found to increase the chlorophyll II level in the host plants (Sujatha and Ammani 2013). Singh et al. (2020) have isolated 10 bacterial strains from the rhizosphere of sugarcane with siderophore production potential, whereas Hussein et al. (2019) have studied the siderophore production potential of rhizosphere fungi associated with Panax ginseng. The fungal species P. commune, associated with P. ginseng rhizosphere, has been reported as a potent siderophore producer (Hussein and Joo 2019). Khamna et al. (2009) have isolated 75 actinomycetes isolates, from the rhizosphere of different medicinal plants, with siderophore production potential. Among actinomycetes strains, Streptomyces spp. are reported as potent siderophore producers (Ref, if any?).

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Biostimulation

Biostimulation is also known as Phytostimulation. It includes the synthesis of phytostimulating hormones by the plant-associated microbes for plant growth promotion. Rhizomicrobes are known to synthesize different phytohormones, namely, auxins, cytokinins, ethylene and gibberellins. Phytohormones synthesized by rhizomicrobes result in plant growth promotion via stress resistance, overproliferation of lateral roots, increased nutrient and water uptake and so on. Rhizomicrobes are reported as potential Indole acetic acid producers (Spaepen and Vanderleyden 2011; Syamala and Sivaji 2017). Singh et al. (2020) have isolated 22 bacterial strains, with indole acetic acid production potential, from the rhizosphere of sugarcane plants. Production of IAA by rhizomicrobes leads to overproduction of lateral roots and root hairs, which further enhances the soil nutrient uptake ability of the plant. Agrobacterium, Rhizobium, Bradyrhizobium, Klebsiella, Pseudomonas and Enterobacter are reported as potential IAA producing rhizobacterial genera (Mohite 2013; Bal et al. 2017). Khamna et al. (2009) have isolated 36 actinomycetes strains, from the rhizosphere of different medicinal plants, with IAA production potential. Among different actinomycetes strains, Streptomyces spp. are reported as potent IAA producers. Besides IAA, some rhizobacterial species such as B. subtilis, P. fluorescens, Pantoea agglomerans and Rhodospirillum rubrum have also been reported to synthesize cytokinins and gibberellins for the plants (Gupta et al. 2015). Ethylene is a plant stress hormone. Under stressful conditions, ethylene hormone halts the important plant cellular processes and leads to premature senescence. 1-Aminocyclopropane-1-carboxylate (ACC) is the precursor of ethylene synthesized by plants in response to environmental stress (Vejan et al. 2016). Rhizobacteria bestow their host plants with stress resistance by synthesizing the ACC deaminase enzyme (Noumavo et al. 2016). The enzyme converts the ACC precursor into α-ketoglutarate and ammonia, thus surpassing the negative effects induced by ethylene hormone under abiotic stress. Rhizomicrobes associated with the rhizosphere of Papaver somniferum and Jatropha are reported as potential ACC deaminase producers (Barnawal et al. 2017). Two rhizospheric P. aeroginosa strains have been found to enhance the synthesis of phytohormones and salicylic acid in the tomato plant (Parasuraman et al. 2020). Bioinoculation of the tomato seeds with the rhizobacterial strains leads to improved seed germination and growth of the tomato plant (Parasuraman et al. 2020). Rhizobacterial strains are also found to be effective in bestowing the improved nutrient uptake and water stress tolerance among plants with high water demands under drought conditions (Pereira et al. 2010). PGPR are known to minimize the adverse effects of drought stress by inducing the production of antioxidant enzymes, hormones or metabolites. Myracrodruon urundeuva plants inoculated with the PGPR A. lipoferum are more tolerant to drought stress (de Oliveira et al. 2018). Significantly lower superoxide dismutase enzyme activity was found in the inoculated plants as compared to the uninoculated ones under stress conditions. Therefore, the bioinoculation of PGPR in crops can be considered an effective biotechnological tool to alleviate different stress effects among crop plants.

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Biocontrol

Biological stress caused by phytopathogens greatly affects the health and yield of plants. To avoid such losses, chemical pesticides and fungicides are being used, which leads to environmental havoc. The phenomenon by which organisms prevent or reduce the severity of the plant diseases caused by phytopathogens is termed biocontrol and the antagonistic microbes are known as biocontrol agents. Biological control seems to be a sustainable approach for plant disease management as improper use of chemical pesticides leads to the development of resistance among phytopathogens as well as ecological contamination (Tariq et al. 2020). Rhizomicrobes are known as potential biocontrol agents (Beneduzi et al. 2012). Successful bioinoculation of potential rhizomicrobes in crop plants would ensure defence against phytopathogens as well as improvement in plant growth and productivity (Parasuraman et al. 2020). Therefore, the application of rhizomicrobes as biocontrol agents seems to be a potential and eco-friendly approach for sustainable plant growth and development. Rhizosphere inhabiting Bacillus and Pseudomonas genera are potential biocontrol agents (Dorjey et al. 2017). Rhizomicrobes suppress the deleterious effects of phytopathogens by following different mechanisms, namely, production of antibiotics, competition for niche and nutrients, production of lytic enzymes and induced systemic resistance. The most common mechanism for biocontrol among rhizomicrobes is, however, the production of antibiotics. A diverse range of antibiotics have been reported from both rhizobacteria and fungi including polyketides, lipopeptides, alcohols, aldehydes, ketones, heterocyclic nitrogeneous compounds, phenazine derivatives, pyrrole derivatives and many more (Gupta et al. 2015; Singh et al. 2017). Different antibiotics suppress phytopathogens through different mechanisms. Most of these antibiotics attack cellular constituents such as cell walls, cell membranes or ribosomes (Singh et al. 2017). Some of the antibiotics also act as stimulants and induce systemic resistance among the plants. Rhizomicrobes are also able to induce systemic resistance among host plants against phytopathogenic bacteria, fungi, viruses, insects and nematodes. Under the influence of induced systemic resistance (ISR), the plant or its parts become more resistant to the damage-causing pathogens. Jasmonate, ethylene, acetoin, homoserine lactones, siderophores, lipopolysaccharides and so on are the main elicitor compounds used by rhizomicrobes to induce systemic resistance among plants and save them from the biological stress (Gupta et al. 2015). Rhizomicrobes are also potential multienzyme producers. They produce different extracellular lytic enzymes such as chitinases, lipases, phosphatases, proteases, dehydrogenase and glucanase which are used to antagonize the growth of phytopathogens directly or indirectly. Singh et al. (2020) have reported enhanced expression of various enzymatic genes, such as chitinases, glucanases, catalase, superoxide dismutase and phenylalanine ammonia lyase, in sugarcane plants inoculated with selected rhizobacterial Bacillus strains. Chitinase and β-glucanase enzymes produced by rhizomicrobes are particularly effective against pathogenic fungi (Vejan et al. 2016). P. fluorescens associated with the rhizosphere of tomatoes has been found to produce chitinase and β-glucanase

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enzymes to suppress the growth of F. udum causing Fusarium wilt (Kumar et al. 2010). Trichoderma sp. associated with the rhizosphere of strawberry has been found to possess antagonistic potential against the causal agents of root rot of strawberry (Ahmed and El-Fiki 2017). Two rhizospheric P. aeruginosa strains have been found to possess significant antagonistic potential against the phytopathogens of tomato, namely, F. oxysporum and Alternaria solani (Parasuraman et al. 2020). Bacillus strains associated with the rhizosphere of the sugarcane plant have been reported to possess antagonistic potential against the sugarcane rot pathogens, namely, Sporisorium scitamineum and Ceratocystis paradoxa (Singh et al. 2020). Khamna et al. (2009) have isolated 23 actinomycetes strains, from the rhizosphere of different medicinal plants, with antifungal potential. Among actinomycetes strains, Streptomyces spp. are reported as potent antifungal agents. Thus, rhizomicrobes can be considered as potential biocontrol agents, thereby reducing the disease incidence and inducing the systemic resistance among plants.

9.5

Conclusions

Rhizomicrobiome represents a complex niche which involves continuous interactions among the host plant and the associated microbes. Such interactions result in improved plant health, productivity and soil fertility. Rhizomicrobes are progressively gaining agricultural and biotechnological relevance owing to their promising plant growth promotion potential. More research is focused on plant growth promoting rhizobacteria (PGPR), whereas rhizosphere-associated fungi are also of huge significance in terms of plant growth promotion characteristics. There is a need to design efficient strategies for successful isolation and utilization of rhizomicrobes as biofertilizers. There exists a gap between the mechanism of plant growth promotion of host plants by PGPR and their application as biofertilizers in agriculture. To overcome this gap, systemic research is needed to be conducted in the area of rhizomicrobiome for a better understanding of their colonization and their complex interactions. Successful harnessing of this underground treasure, termed as plant growth promoting rhizomicrobes, as biofertilizers, biostimulants and biocontrol agents shall prove to be a big contribution towards sustainable development in general and sustainable agriculture in particular. Acknowledgements The authors are thankful to the Department of Biotechnology, Govt. of India for its facilities. The infrastructural facilities created in the School under RUSA, PURSE, FIST and SAP are also acknowledged.

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Synthetic Biology Tools in Cyanobacterial Biotechnology: Recent Developments and Opportunities

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Krishna Kumar Rai, Ruchi Rai, Shilpi Singh, and L. C. Rai

Abstract

Cyanobacteria are ubiquitous microorganisms that play a significant role in the maintenance of the earth’s ecology. Owing to the smaller and completely sequenced genome, some strains have emerged as appropriate candidates for manipulating their genetic sequences to enhance growth and photosynthesis under distinct environmental fluctuations. Synthetic biology tools have arisen as an indispensable means for scaling up the natural circadian rhythm of prokaryotes and eukaryotes, thus improving the physiological and metabolic processes to promote their growth under adverse environmental conditions. Although the availability of synthetic biology tools for engineering multiple pathways in cyanobacteria is still limited, in the past few years significant progress has been made in developing genetic tools including promoters, sRNA, RBS, riboswitches and CRISPR (clustered regulatory interspaced short palindromic repeats)/Cas-9 systems for engineering cyanobacteria with improved biomass production and product development. Systematic rewiring of physiological, biochemical and molecular pathways may significantly improve the growth and production of engineered cyanobacteria under stressful environments. In this chapter, recent advancement in synthetic biology tools and their application in cyanobacteria for sustainable biotechnologies is reviewed. Furthermore, it also provides valuable insights into their future developments.

K. K. Rai · R. Rai · S. Singh · L. C. Rai (*) Molecular Biology Section, Centre of Advanced Study in Botany, Institute of Science, Banaras Hindu University, Varanasi, Uttar Pradesh, India e-mail: [email protected] # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2022 U. B. Singh et al. (eds.), Re-visiting the Rhizosphere Eco-system for Agricultural Sustainability, Rhizosphere Biology, https://doi.org/10.1007/978-981-19-4101-6_10

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Introduction

Cyanobacteria are an evolutionarily ancient and ecologically important diverse clade of photosynthetic prokaryotes contributing significantly towards primary productivity (Banerjee et al. 2013; Yadav et al. 2018). The arrangement of chloroplasts of higher plants has been postulated to be the product of endosymbiotic uptake of cyanobacteria (Singh et al. 2013). Consequently, they are recognized as ubiquitous model organisms for contemplating physiological processes such as photosynthesis, electron transport chain and biochemical process that are considerably similar to most of the eukaryotic algae and higher plants (Tan et al. 2015). Recently, the CO2 concentrating mechanism of cyanobacteria has been shown to be involved in the improvement of growth and productivity of various agricultural crop plants (McGrath and Long 2014); however, it is still a daunting task for producing ample food in changing climate to bridge demand and supply gap of the ever-growing population (Singh et al. 2013). Substantial research investigations have been made to characterize cyanobacterial genomes using next-generation sequencing techniques and sequence assembly tools (Tan et al. 2015). These investigations have revealed novel information about cyanobacterial genes and their functions which can be exploited to modulate the metabolism of cyanobacteria for the biosynthesis of desired products using advanced synthetic tools (Carter and Warner 2018). Genome editing through various sitespecific nucleases such as zinc-finger nucleases (ZFNs), transcription activator-like effector nucleases (TALENs) and newly identified clustered regulatory interspaced short palindromic repeats (CRISPR)-CRISPR associated protein (Cas) has provided a singular platform for gene editing. Despite the technological advancement and increased application, few attempts have been made in the implementation of the CRISPR-Cas9 system for cyanobacterial improvement (Sengupta et al. 2018). The major constraint for its application in cyanobacteria is to develop a rapid and robust protocol of genetic transformation which can be leveraged for improving the photosynthetic process in crop plants which may in turn improve their growth and productivity under climate extremes. Synthetic biology is an emerging discipline that intercepts biotechnology and advanced molecular biology from an analytical schematic approach to manipulate host cell metabolism and regulatory systems with high efficiency (Hagemann and Hess 2018). Initially, research involving synthetic biology was mainly focused on model species like E. coli and yeast. However, the exploitation of synthetic biology has been lagging in developing an efficient cyanobacterial transformation system (Johnson et al. 2016). While cyanobacteria are an ideal candidate for metabolic engineering, a relatively small number of cyanobacterial strains have been used as models for example, Synechococcus elongatus PCC 7942, Synechocystis sp. PCC 6803 and Nostoc sp. PCC 7120. Owing to fast growth rates, capacity to withstand high light intensities and elevated temperatures, Synechococcus PCC 7002, S. elongatus UTEX 2973 and S. elongatus PCC 11801 are further included in this list (Johnson et al. 2016). This chapter is an attempt to dissect recent advancements

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and bottlenecks that hinder efficient cyanobacterial transformation via the implementation of ultra-throughput genome editing CRISPR-based tools.

10.2

Development of BioBricks for Tailoring Cyanobacterial Genome

BioBricks are the arrangement and/or reconfiguration of new/existing biological parts that can be efficiently mobilized into living organisms (Lindblad 2018). These BioBricks are the intersecting elements involved in the precise modulation of genetic engineering principles for manipulating host cells. These BioBricks are also referred to as ‘Genetic toolboxes’ which are the main players catalysing manipulation of the genome with high efficiency (Sengupta et al. 2018). BioBricks include a wide variety of genetic tools being developed to carry out both primitive and advanced molecular research in a biological system such as inducible or constitutive promoters, plasmid or shuttle vectors, ribosome binding site (RBS), riboswitches, CRISPR-Cas systems, small RNA mediated tools which have been exploited efficaciously for gene editing to stimulate stress tolerance and metabolic manipulations in E. coli, yeast and in model cyanobacterial species (Santos-Merino et al. 2019). Cyanobacterial synthetic biology research has been accelerated in the last 8–10 years as delineated by an increasing number of publications. Efforts are on way to strengthen genetic toolboxes in cyanobacteria, which will be discussed in the following sections. An overview of genome editing and the application of various synthetic biology tools in metabolic engineering of cyanobacteria is summarized in Fig. 10.1.

10.2.1 Inducible and Constitutive Promoters Inducible promoters can regulate the expression of specific genes under the influence of certain inducers, whereas constitutive promoters are programmed to facilitate persistent transcription of endogenous genes in an unregulated manner (Liu and Pakrasi 2018). A promoter is considered an ideal promoter if it is capable of generating a predictable response at a specific concentration of inducer or repressor and should be stable/lie dormant under normal conditions of growth and development (Behle et al. 2019). A plethora of research has indicated that most of the inducible promoters have metal-binding activity that modulates host cell metabolisms under distinct environmental stresses which otherwise may cause protein denaturation (Zess et al. 2016). For example, some promoters named coaA and PnrsB from Synechocystis sp. PCC 6803 and Psmt and PisiAB from Synechococcus sp. PCC 7942 were significantly induced under various heavy metal stresses. An isopropyl-β-D-thiogalactoside (IPTG) induced promoter with a repressed LacI promoter has been shown to differentially regulate the genes involved in photosynthesis and nitrogen fixation in S. elongatus PCC 7942. Interestingly, E. coli promoter L03 induced by anhydrotetracycline (aTc) was able to regulate the expression of genes

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Fig. 10.1 Strategy for engineering cyanobacterial genome incorporating both computational and experimental aspects by exploiting novel synthetic biology tools. First, the synthetic biological parts are identified, tailored and tested for enhancing light-driven product synthesis in cyanobacteria. The models are then further refined based on the data sets generated to create efficient/improved synthetic biology toolkits. These advanced toolkits are then used to modulate the expression of genes/proteins of metabolic pathways to increase light-driven product synthesis in cyanobacteria and at the same time minimize the instability in the engineered strains. CBB, Calvin-BensonBassham cycle; RBS, Ribosome binding sites; dCas9, CRISPR-associated protein 9; FACS, Fluorescence-activated cell sorter

involved in the photosynthetic process, circadian rhythm and stress defence pathway (Jin et al. 2019). Simultaneously, overexpression of T03 promoter with tetR repressor causes significant induction of T03 promoter up to 200-fold in Synechococcus sp. PCC 7002, 7942 and Synechocystis sp. PCC 6803, thus confirming its wide adaptability (Zess et al. 2016). Researchers have also attempted to improve cyanobacterial growth and biomass production by stimulating the uptake of xylose or glucose by overexpressing arabinose-inducible promoter PBAD (Dong et al. 2018). Additionally, heterologous expression of E. coli PrhaBAD promoter which is induced in the presence of rhamnose in Synechocystis sp. PCC 6803 causes significant induction of the RhaS transcription factor which in turn stimulates the glucosexylose-rhamnose metabolic pathway leading to improved growth and biomass production (Santos-Merino et al. 2019). Nonetheless, the feasibility and efficiency of these promoters need to be further validated and evaluated in other cyanobacterial species. In oxygenic photosynthetic cyanobacteria, the oxygen-sensitive enzymes/ metabolites such as dehydrogenase significantly alter the production of 1-butanol more readily compared to anoxic conditions (Immethun et al. 2016). This concern was overcome by constructing two strong cyanobacteria-specific promoters by employing the fumarate and nitrate reduction (FNR) system of E. coli. In an attempt,

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the fnr gene system was introduced in Synechocystis sp. PCC 6803 to develop an FNR-activated promoter that was able to induce the expression of concerned genes under oxygen-free conditions (Immethun et al. 2016). Another attempt involved the introduction of the dark sensing protein Cph1 of Synechocystis in E. coli, which is capable of phosphorylating histidine kinase resulting in the modulation of transcriptional regulation of the OmpR gene in E. coli leading to its activation under dark conditions (Sun et al. 2018). Furthermore, several researchers have shown that the most effective way to design promoters is by modulating the interaction between response regulators (RRs) and transcription factors (TFs) (Vasudevan et al. 2019). Huang et al. (2016) engineered slr1037 and sll0039 (RR encoding genes) and TF encoding gene Sll1626 that tremendously enhanced the tolerance against 1-butanol and fatty acid biosynthesis in some cyanobacterial strains. Constitutive promoters such as PpsbA2, PrnpB and PcpcB have been systematically elucidated in cyanobacteria for producing fuels and chemicals by regulating the expression of genes of various metabolic pathways (Yao et al. 2015; Wang et al. 2017). In addition, several attempts have also been made to develop new promoters in various cyanobacteria either by modifying existing promoters or by using various computational approaches and online databases. For instance, Sun et al. (2018) significantly modified the tandem promoter rRNA from Synechococcus sp. PCC 7942 using Ps promoter from E. coli which increased the production of soluble proteins compared to their native form. Similarly, several endogenous promoters such as Pcpc560 (from PcpcB) and PpsbA2S (from PpsbA2) have been modified/ optimized to efficiently regulate the production of functional proteins; these were also able to regulate the expression of several reporter genes (Sun et al. 2018). Furthermore, several researchers have also confirmed the superiority of truncated promoters over their native form (Behle et al. 2019). Some strong promoters such as Pcpc560 and Prbc designed by using bioinformatic tools in Synechococcus sp. PCC 7002 and Synechocystis sp. PCC 6803 were able to regulate gene expression up to eightfold compared to control cells. Additionally, the efficiency of promoters involved in regulating genes of the photosynthetic pathway was examined using yellow fluorescent protein as a probe. This study led to the discovery of promoter Psll1626 which exhibited strong activity (up to 1000-fold) compared to the native PrbcL promoter (Miao et al. 2017).

10.2.2 Optimizing RBS Modifications The ribosome binding site (RBS) is the sequence located upstream of the start codon of mRNA and specifically involved in the recruitment of ribosomes during translation. RBS has the ability to affect gene expression in terms of translational efficiency up to 10,000-fold (Sengupta et al. 2018; Lindblad 2018). It is essential for modulating the coordinated translation of several downstream genes by facilitating the interaction between ribosome and Shine-Dalgarno (SD) sequences (Wendt et al. 2016; Sun et al. 2018). Bacterial transcription and translation systems primarily consist of promoters, terminators, coding sequences (CDS) and RBS sequences

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(Singh et al. 2016). Among all, RBS sequences are the ones that strategically perform critical binding between mRNA and ribosomes. RBS engineering is mainly achieved by changing the nucleotide sequences present upstream of the START codon through transgenic approaches. Upstream of the START codon through transgenic approaches. Some efforts have been made during the last couple of years to engineer RBS sequences in both algae and cyanobacteria for enhancing the productivity of several metabolic pathways (Sakamoto et al. 2018). Furthermore, attempts have been made to engineer RBSs to increase the production of 2,3-butanediol in Synechococcus sp. PCC 7942 by improving the transcription of three genes, namely, alsS, alsD and adh, of 2,3-butanediol biosynthesis pathways (McEwen et al. 2016). Further, Zhou et al. (2016) were also able to stimulate the biosynthesis of 2,3-butanediol in Synechococcus sp. PCC 7942 by employing different RBS promoters with contrasting translation competencies and reported approximately 1.8–2.0-fold increase in the final production. Attempts are on to modify the existing toolboxes especially promoter and RBS sequences to optimize the production. Veetil et al. (2017) selected the content-specific RBS features in one of the strongest plant promoters, namely, strongest plant promoters, namely, PpsbA from pea, and transferred it into Synechosystis sp. PCC 6803 which resulted in increased expression of ethylene-forming enzyme, thereby enhancing ethylene production up to threefold. Likewise, Wang et al. (2017) developed a PpsbA promoter targeting RBS to enhance the expression of the limonene synthase (LS) gene in Synechococcus sp. PCC 7942, thus accelerating the production of limonene by 20–30-fold. Tailoring RBS sequences can have an erratic effect on specific gene functions which can instigate severe repercussions on the expression of genes/proteins in different microorganisms (Carroll et al. 2018). Therefore, in order to achieve the desired RBS modifications, one needs to validate the competency of edited RBSs by performing several in silico-based prediction programs such as RBS calculator, RBS designer and UTR designer that efficiently use statistics based thermodynamic algorithm to predict the efficiency of specific ribosome-mRNA pairs (Vijay et al. 2019). Advancement in these tools has facilitated the development of RBS libraries per se in Synechococcus sp. PCC 7002 and Synechocystis sp. PCC 6803 (Thiel et al. 2018). The efficiency and experimental validation for all the three tools have been evaluated and predicted based on the determination coefficient (R2) in cyanobacteria.

10.2.3 Riboswitches Mediated Regulation of Gene Expression Riboswitches are cis-acting elements located at 50 -untranslated regions (50 -UTR) with the ability to regulate the expression of mRNA upon binding to small molecules called ligands. However, in the absence of these ligands, the conformation of riboswitches is altered which may lead to inhibition of transcription/translation due to self-cleavage of target mRNA (Sengupta et al. 2018; Klahn et al. 2018; Taton et al. 2017). Riboswitches have presented themselves as an exceptional tool that efficiently regulates gene expression with a high degree of modularity. Furthermore,

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they are also able to induce the expression of several genes within a short time even in the absence of an inducer/enhancer, thereby abating their leaky expression (Ohbayashi et al. 2016). Singh et al. (2018) successfully manipulated theophylline-dependent riboswitch for controlling gene expression in distinct microbial systems such as Prochlorococcus marinus, Synechococcus sp. PCC 7335 and Synechocystis sp. However, their use in cyanobacteria is well known where Nakahira et al. (2013) introduced a modified theophylline-dependent riboswitch that regulated the expression of proteins in Synechococcus sp. PCC 7942 even in the absence of ligand. Additionally, this riboswitch has also been exploited in other cyanobacterial species such as Synechocystis PCC 6803, Leptolyngbya BL0902, Nostoc sp. PCC 7120 and Anabaena sp. PCC 7120 (Taton et al. 2017) where the modified theophylline riboswitch under the control of transcriptional repressors resulted in reduced expression of genes. A novel and native cobalamin-responsive riboswitch capable of functioning well has also been discovered in Synechocystis sp. PCC 7002 (Perez et al. 2016). However, its implementation remains elusive in those cyanobacterial species which are not cobalamin autotrophs. In addition, recently theophyllinedependent riboswitch was also engineered in Synechococcus sp. PCC7942 to control the expression of ADP-glucose pyrophosphorylase (glgC) expression which resulted in a 40–300% increase in the intracellular concentration of glgC and glycogen synthesis (Chi et al. 2019). Subsequently, the modified theophylline-responsive riboswitch (theophylline riboswitch) resulted in decreased expression of NADPdependent sorbitol-6-phosphate dehydrogenase (S6PDH) compared to simple trc promoter that resulted in four- to fivefold decrease in the rate of sorbitol production in Synechocystis sp. PCC 6803 (Chin et al. 2019). However, efforts are constantly being made to discover new riboswitches detecting metabolites such as TPP, FMN, queuosine, roseoflavin and cyclic dinucleotides (Cano et al. 2018). Nonetheless, their suitability, efficiency and genetic stability in cyanobacteria need to be experimentally verified.

10.2.4 Small RNA (sRNA) as Functional Tools Bacterial sRNA belongs to a class of non-coding RNA of approximately 50–300 nucleotides that are able to regulate mRNA via proper or improper base pairing (Jagadevan et al. 2018). Small RNA (sRNA) aided synthetic biology tools have shown to be effective in regulating important cellular and biological processes such as replication, virulence and plasmid regulation in bacteria (Chappell et al. 2015). In addition, sRNAs are also able to regulate various signal transduction processes at distinct developmental stages that effectively improve their growth and adaptability under different abiotic stresses (Brenes-Álvarez et al. 2016). Furthermore, strategic engineering of sRNA can help in designing effective regulatory tools by removing non-essential genes to target distinct metabolic pathways having a toxic effect on host cells (Brenes-Álvarez et al. 2016). Nowadays, sRNA is being explicably used and functionally characterized in cyanobacteria, but to date fewer studies have

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reported their successful application as a genetic tool (Pei et al. 2017). For instance, Abe et al. (2014) successfully exploited sRNA-based genetic tool for improving the translation of cis-repressive mRNA using a trans-activating RNA. Additionally, they also devised and efficiently optimized the MicF and chaperone Hfq system in E. coli utilizing a trans-activating sRNA scaffold molecule that significantly improved intermolecular hybridization with cis-repressive sRNA (Dersch et al. 2017). A complete list of researchers who have used sRNA as genetic tools for engineering metabolic pathways in cyanobacteria is compiled in Table 10.1. Hu et al. (2017) identified an antisense RNA (asRNA) named RblR which is 113 nucleotides in length in Synechocystis sp. PCC 6803 that exhibited appreciable complementarity to its target gene rbcL, thus efficiently modulating its expression under various abiotic stresses. Simultaneously, Ueno et al. (2017) used this tool to activate the transcription of the cyAbrB2 gene for enhancing glycogen biosynthesis in Synechocystis sp. PCC 6803. Overexpression of CoaR resulted in the downregulation of slr0847 (coaD) and slr0848 operon, thereby enhancing tolerance of Synechocystis sp. PCC 6803 to 1-butanol and acting as a negative regulator for the synthesis of CoA (Sun et al. 2017). Georg et al. (2017) modified the photosynthetic apparatus of cyanobacteria by using trans-acting IsaR1 sRNA which induced oxygenic photosynthesis and improved survival under iron-deficient conditions. Furthermore, Srivastava et al. (2017) have also reported the inability of a transencodings RNA in regulating transcription of sigJ, a sigma factor encoding gene in Anabaena PCC 7120. Knocked down of this trans-encoding RNA enhanced the expression of sigJ gene which in turn improves the tolerance of Anabaena PCC 7120 against photooxidative stress. Analysis of transcriptome through comparative approach identified 119 upregulated genes of which slr0007 significantly enhanced the tolerance of Synechocystis sp. PCC 6803 by stimulating the synthesis of lipopolysaccharide (Bi et al. 2018). Simultaneously, Sun et al. (2018) devised two new sRNA mediated genetic tools in Synechocystis sp. PCC 6803 using paired termini RNAs (PTRNAs) and Hfq-MicC scaffold RNA analogous to E. coli which were able to knock down the expression of target genes up to 90% leading to an increased synthesis of malonyl-CoA up to 50%. Most recently, Olmedo-Verd et al. (2019) functionally characterized a novel sRNA in Nostoc PCC 7120 named as_glpX that encodes two important enzymes of the Calvin cycle, namely, sedoheptulose 1,7 bisphosphatase and fructose 1,6 bisphosphatase (SBPase). Transcription of as_glpX is induced in the early differentiation process of heterocyst development and its overexpression leads to decreased expression of glpX mRNA. So, they targeted as_glpX mRNA as a tool to shut down the process of CO2 fixation to regulate metabolic transformation in Nostoc heterocyst. Besides their role in posttranscriptional regulation, sRNA has also been known to efficiently regulate gene expression under extreme climatic conditions, thus strengthening their growth and biomass by enhancing their abiotic stress tolerance (Pei et al. 2017). These technological advancements together with in silico approaches have remarkably facilitated the identification of several sRNAs that are able to differentially regulate gene expression under various biotic and abiotic stresses (Giner-Lamia et al. 2018; Sun et al. 2018).

Synechocystis sp. PCC 6803 Anabaena PCC 7120 Synechococcus elongatus PCC 7942 Synechococcus sp. PCC 7002 A. platensis NIES39

Cyanobacterial species Synechocystis sp. PCC 6803 Synechocystis sp. PCC 6803 Arthrospira platensis Synechocystis sp. PCC 6803

GSMApNIES-39

iSyp821

Manually created a stoichiometric model iJB785

Gluconeogenesis and carbon fixation TCA and pentose phosphate pathways

Photosynthesis and oxidative phosphorylation processes Carbon and nitrogen metabolism Production of high-value chemicals

TCA cycle, Calvin-Benson cycle

imSyn716

iSynCJ816

Glycogen metabolism

Target genes/metabolites Calvin cycle and photorespiratory system Metabolic pathways

iAK888

CycleSyn

Genome-based model imSyn617

Enhanced glycogen and lipid synthesis under nitrogen depletion Enhanced glycogen production under nitrogen deprivation condition

Enhanced photosynthesis leading to increased metabolism

Improved growth

Increased CO2 fixation up to 35%

Enhanced glyoxylate metabolism and corrinoid biosynthesis

Functional role Improved growth and enhanced synthesis of biochemicals Improved pyruvate metabolism and cellular growth Increased glycogen biosynthesis

Table 10.1 List of recently developed genome-scale models (GSMs) in cyanobacteria

Flux balance analysis Flux balance analysis

Flux balance analysis Flux balance analysis 13 C-metabolic flux analysis

Algorithm used 13 C-metabolic flux analysis Flux balance analysis Flux balance analysis 13 C-metabolic flux analysis

Yoshikawa et al. (2015)

Qian et al. (2017a)

Malatinszky et al. (2017) Broddrick et al. (2016)

References Hendry et al. (2019) Sarkar et al. (2019) Klanchui et al. (2018) Gopalakrishnan and Maranas (2015) Joshi et al. (2017)

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10.2.5 Utilization and Function of Reporter Genes An efficient way to detect and validate synthetic biology tools in terms of their reproducibility and efficacy is by applying a suitable reporter gene. The reporter genes facilitate sophisticated detection of important biological circuits without causing any lethality to target organisms (Taton et al. 2017). The efficacy and reproducibility of any reporter gene depend upon its localization ability and fluorescence intensity. The reporter genes such as luciferase and fluorescent proteins are most frequently and robustly used in most bacterial systems. On the contrary, in the cyanobacterial system, lux operon is well studied and used for predicting the realtime location of genes (Thiel et al. 2018). Furthermore, several reporter genes have been devised and functionally characterized as physical and metabolic sensors based on input signals sensed by them (Immethun et al. 2016). Physico-chemical sensors comprise environmental signals such as light, temperature and CO2/O2 levels; for example, a two-component system associated histidine kinase (CcaS) reporter is an endogenous reporter present in Synechocystis sp. PCC 6803 which gets activated in response to green light and deactivated upon exposure to red light (Brand and Owttrim 2017). Likewise, an oxygen responsive genetic circuit has also been developed in Synechocystis sp. PCC 6803 using fumarate and nitrate reduction (FNR) system which was capable of working under both aerobic and anaerobic conditions and efficiently transcribed nifHDK under oxygen-deprived conditions, thus stimulating the transcription of fnr gene (Immethun et al. 2016). Reporter genes directing arabinose signalling have also been created using arabinose-responsive promoter (PBAD) in Synechocystis sp. PCC 6803. Similarly, reporter genes regulating gene expression of various metabolic pathways have also been documented in Synechocystis sp. PCC 6803. Expression of NtcA-responsive reporters under the influence of NtcA-activated promoters along with RNA polymerase II promoters and sigma factor efficiently regulated the expression of flavinbinding fluorescent protein ( fbfp), thus stimulating the conversion of iso-citrate to 2-oxoglutarate under varying nitrate concentrations (Immethun et al. 2017). More recently, Cotterill et al. (2019) developed a Cyclops-7 phycocyanin reporter gene for measuring intracellular phycocyanin concentration in cyanobacteria. The developed Cyclops-7 phycocyanin reporter gene reliably predicted phycocyanin levels at different cyanobacterial biovolume. Likewise, Kumar et al. (2019) exploited the gfp-reporter construct fused with nifD and nifH genes to activate the transcription of hglD and hglE genes involved in the differentiation of the heterocyst and glycolipid layer production.

10.3

Advancing Cyanobacterial Transformation Through the CRISPR-Cas System

Genome editing tools based on CRISPR-Cas systems have recently gained much attention for manipulating gene expression in various organisms. This technique was primarily identified in Streptococcus pyogenes which protects them from various

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pathogenic microorganisms by stimulating their adaptive immune response (Ungerer and Pakrasi 2016). In recent years, the CRISPR-Cas systems have reformed the genetic engineering technology which uses spacer sequences that guide CRISPR RNA (crRNA) and trans-activating crRNA (tracrRNA) to induce double-stranded break in target DNA (Wendt et al. 2016). In eukaryotes, the CRISPR-Cas system is being widely used to engineer crop plants against various biotic and abiotic stresses, whereas its implication in prokaryotes such as cyanobacteria is still lagging (Mougiakos et al. 2018). The implementation of the CRISPR-Cas system in cyanobacteria was incepted by targeting nonbleaching protein A (nblA) mutation which impedes the depigmentation process by stimulating phycobilisome degradation under nitrogen deficit conditions (Wendt et al. 2016). The depigmentation process in cyanobacteria is an easily recognizable trait developed when all nblA copies are mutated, thus presenting themselves as an excellent observable phenotype during the segregation process. Therefore, the cyanobacterial scientific community began exploiting the CRISPR-Cas system for advancing the genome editing process. In their study, a group of researchers observed that approximately 70% of CRISPR transformed cells were able to segregate without using selection markers (Behler et al. 2018). Nonetheless, the CRISPR-Cas system has substantially impacted the field of cyanobacterial biotechnology by precisely engineering its genome and improving its growth and biomass under stress conditions (Masepohl et al. 1996; Barrangou and Horvath 2017). In addition, the efficiency of the CRISPR-Cas system was also validated by another research group where they have reported that the efficiency of homologous recombination was significantly improved in conjunction with the CRISPR-Cas system genome editing process in S. elongatus sp. PCC7942 (Huang et al. 2016). Following successful validation in cyanobacteria, Li et al. (2016) employed the CRISPR-Cas system for stimulating the production of succinate compounds with multiple industrial applications. For this, they used the CRISPR-Cas system to mutate the glgC gene encoding glucose-1-phosphate adenylyl transferase enzyme that stimulates glycogenesis by diverting carbon away from succinate which resulted in increased synthesis of succinate. Furthermore, the same group also generated a knock-in mutant comprising ppc and gltA genes using the CRISPR-Cas system in the glgC locus which resulted in a twofold increase in succinate production by improving the tricarboxylic acid (TCA) cycle (Behler et al. 2018). The above findings undeniably confirmed the practical applicability of the CRISPR-Cas system for cyanobacterial engineering. Apart from their role in improving gene editing efficiency, CRISPR-Cas systems are also impeccably used in the improvement of homologous recombination in cyanobacteria by generating short homology arms of about 400 bp compared to previously used 700–1000 bp arms. The advantage of using a short arm is that it opens up the possibility of integrating genes having shorter genomic target sites, thus efficiently confronting random recombinational events that otherwise have severe repercussions on the nature and behaviour of host performance. Additionally, the CRISPR-Cas system uses a small template DNA for genome editing as well as for homologous recombination from 2000 ng to 200–300 ng (Fokum et al. 2019).

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The CRISPR-Cas system has some limitations in cyanobacteria and needs further refinement before it suitably replaces traditional engineering techniques. One of the major constraints in the application of the CRISPR-Cas system in cyanobacteria is the high rate of false-positive colonies for desired DNA modification. Several findings on cyanobacterial transformation have reported around 40–60% mutation in the CRISPR-transformed colonies (Wendt et al. 2016; Xiao et al. 2018). In addition, the CRISPR-Cas system has also been reported to be toxic in some cyanobacterial species like S. elongatus, which could be due to the lethality of Cas9 protein or the unavailability of homologous DNA for the repair process (Xiao et al. 2018). In the meantime, efforts are being diverted towards developing a target-based inducible system in cyanobacteria to reduce the lethal effect of the Cas9 system by exploiting a new CRISPR-based Cpf1 system (CRISPR from Prevotella and Francisella 1) which is able to improve the transformation efficiency with minimum leakage (Behler et al. 2018; Sun et al. 2018). Given the importance of the CRISPR-Cas system for genome editing, researchers are now exploiting a new variant of Cas9 for cyanobacteria named Cpf1 (previously known as Cas12a protein), a non-toxic RNA-directed dsDNA nuclease that generates a cohesive cut using crRNA (Higo et al. 2017). This CRISPR-Cpf1 system has been effectively applied in Synechococcus sp. PCC 7942, Synechococcus sp. PCC 2973, Synechocystis sp. PCC 6803 and more recently in Anabaena PCC 7120 for generating mutants and knockouts without having any lethal effect on the host (Niu et al. 2018; Santos-Merino et al. 2019). CRISPR-Cpf1 has also been successfully used to upregulate the expression of various genes by stimulating transcription factors and enhancer sequences (Higo et al. 2017). An overview of the CRISPR-Cas9 system and its implementation in improving cyanobacterial growth and metabolism is depicted in Fig. 10.2.

10.4

Genome-Scale Metabolic Models

Genome-scale models (GSMs) are computation-based tools that are able to simulate gene-protein interaction to predict metabolic fluxes for various ‘OMICS’-based studies. These models can be easily generated using genomic sequences and their feasibility can be readily validated by various computational approaches (O’Brien et al. 2017). Some recent findings on the automation of genome-based models in cyanobacteria have been documented; nonetheless, they are way behind compared to heterotrophic microorganisms (Gudmundsson et al. 2017). Heterologous pathways in cyanobacteria have been targeted using a stoichiometrically designed model for enhancing the production of alcohol, ethylene and isoprene (Knoop and Steuer 2015). The genome-based models in Synechocystis sp. PCC 6803 have been used for increasing the production of alcohols, terpenes and fatty acids by improving fermentation and beta-oxidation processes on the one hand and maintaining an adequate balance of intracellular ATP and NADPH through exterminating NADH sinks on the other hand (Shabestary and Hudson 2016). The cyanobacterial metabolic network has been integrated and reconstructed for enhancing the production of

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Fig. 10.2 Overview of CRISPR-Cas system for engineering cyanobacteria. The figure represents the systematic layout of CRISPR systems including locus and domains. This system uses crRNA and trans-activating crRNA guided by spacer sequences to induce double-stranded break using Cas proteins. The construct containing essential elements is then used to induce double-stranded break in cyanobacteria for cleaving the desired DNA sequence. Following transformation, the doublestranded break is then repaired by either homologous recombination or non-homologous end joining method as mediated by template plasmid. The selection of respective transconjugants is done on Kanamycin supplemented agar plates and the positive colonies are then streaked on BG11 medium supplemented with Kanamycin for the selection of mutants with desired traits

limonene and isobutyraldehyde (Mohammadi et al. 2018). Similarly, Wang et al. (2017) devised a computational tool to monitor limonene flux and photosynthesis rate and concluded that limonene synthase is the key enzyme involved in the limonene synthesis pathway. Metabolic flux analysis based on 13C between normal and recombinant Synechococcus sp. PCC 7942 has outlined important genes involved in glycolysis, as well as associated pathways and overexpression of these genes, resulting in the increased production of pyruvate kinase (Jazmin et al. 2017). In many cyanobacterial species such as Anabaena PCC 7120 and Synechocystis sp. PCC 6803, approximately 50% of proteins are uncharacterized ‘hypothetical proteins’ (Pandey et al. 2013; Agrawal et al. 2015; Rai et al. 2019). However, proteomics studies have been able to identify several hypothetical proteins that are up-accumulated in response to stress conditions which can be further classified based on cellular and biochemical functions they perform using interaction studies. Additionally, these interaction studies have led to the identification of genes linked to the metabolic and other signalling pathways (Agrawal et al. 2014). Inclusion of these studies along with genome-based models will facilitate the detailed characterization of these hypothetical proteins, discover new signalling pathways, establish a mechanistic link between metabolic pathways and thus contribute significantly towards the

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engineering of cyanobacteria for biotechnological application (Agrawal et al. 2017, Chaurasia et al. 2017; Singh et al. 2017; Shrivastava et al. 2016). In this context, some attempt has been made to provide functional insight into various metabolic pathways by targeting essential genes via genome-scale models in Synechococcus sp. PCC 7942, thus constructing sophisticated models to provide a better understanding of the nucleic acid metabolism (Qian et al. 2017; Abernathy et al. 2019). Similarly, Klanchui et al. (2018) have constructed a genome-scale model known as iAK888 for predicting cellular/biochemical behaviour as a tool to enhance glycogen production that could eventually increase bioethanol production in Arthrospira platensis. The simulated model iAK888 can further be modified and used in other cyanobacterial species for enhancing growth, biomass and biofuel production; however, it requires experimental validation before its application. Most recently, Hendry et al. (2019) have reported solar-based production of biofuels/biochemicals by generating a genome-based mapping model, namely, imSyu593, in Synechocystis sp. PCC 6803. The constructed model was an improvement over previously designed imSyn617 that significantly improved not only carbon metabolism (up to 96%) but also increased the rate of carbon uptake, thus increasing the biomass of Synechococcus sp. PCC 2973 (Hendry et al. 2019). Altogether, the above-mentioned research findings demonstrated the potential role of genome-based models and their application in synthetic biology (Table 10.1).

10.5

Development of Modular Cloning Suite for Cyanobacterial Transformation

Synthetic biology tools have revolutionized the engineering of the microbial genome by remodelling the traditional method of recombinant DNA technologies and accelerating the analysis, assembly and synthesis of metabolic pathways/compounds (Vasudevan et al. 2019). Compared to the traditional method of genetic engineering such as chemical, mechanical and electrical, synthetic biology involves contemplation, dissolution and systemization of basic biological elements such as promoters, terminators, RBS, riboswitches and sRNA to develop an efficient biological system with high accuracy (Santos-Merino et al. 2019). Owing to its small genome size and the availability of the complete genome sequence, the precise and efficient synthetic engineering of cyanobacteria can result in the sustainable production of essential metabolites and biofuels for agricultural and industrial applications (Singh et al. 2016). The upper hand of synthetic engineering involves high accuracy, increased pyramiding of transgene and enhanced gene expressions, thus eventually reducing the risk of epigenetic modifications and off-target contaminations (Zess et al. 2016). One of the fundamental aims of synthetic biology mediated tools is to engineer the existing metabolic pathways for enhancing the bioproduction of high-value metabolites/compounds which is otherwise impossible to be achieved by traditional cloning methods (Du et al. 2018). To expedite high-throughput cloning in cyanobacteria, a robust and powerful approach called the golden gate cloning system has been described which is capable

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of assembling several genes in one construct (Nagel 2019). This golden gate system involves the use of IIS restriction enzymes capable of digesting nucleic acid away from their restriction sites with the probability of generating 44 nucleotide overhangs with a high degree of ligation to facilitate the assembly of multiple genes in one construct in a systematic orientation to perform high-throughput cloning in cyanobacteria (Sebesta et al. 2019). In addition, the technique also facilitates the easy construction of multiple combinations by using the same four-nucleotide overhangs to both 30 and 50 ends. This new modular cloning (MoClo) method has been widely adopted in bacteria, plant and animal systems and has significantly improved the efficiency of assembling different genetic parts with complex vectors in a highly economical and accessible way without the application of any proprietary tools and reagents (Engler et al. 2014). However, in cyanobacteria development of a modular cloning suite has been adopted by Vasudevan et al. (2019) by modifying the plant golden gate cloning toolkit. They designed vectors for assembling different individual genetic elements including 21 terminators and 12 constitutive and 33 inducible promoters in Synechocystis sp. PCC 6803 and Synechococcus sp. UTEX 2973 and efficiently merged them with CRISPR/Cas system to generate knock-out mutants. They constructed a robust CyanoGate system linking cyanobacteria with algal and plant systems by integrating golden gate MoClo syntax and genomic libraries of plants from different platforms for the characterization of different genetic elements such as promoters, terminators and RBS. Further, they also constructed level T acceptor vectors for scaling up the integrative or replicative transformation process and generated both knock-in and knock-out mutants more efficiently. Above workers (Vasudevan et al. 2019) assembled T vectors with eYFP expression cassette (Pcpc560-eYFP-TrrnB) to generate pPMQAK1-T-eYFP and pSEVA421-T-eYFP trans-conjugates in Synechocystis. The expression cassettes were then assembled on the CRISPRi system to study gene repression by designing small regulatory RNA to recruit Hfq protein (highly conserved among bacteria). The trans-conjugates expressing only sgRNA showed no reduction in eYFP expression. On the contrary, the trans-conjugates carrying Cas9 construct showed a 40–90% reduction in the expression as observed previously for Synechococcus PCC 7002 and Synechocystis, thus confirming the utility of CyanoGate kit with CRISPRi system (Vasudevan et al. 2019). Overall, the designed CyanoGate-based MoClo kit efficiently improved the availability of genomic elements in cyanobacteria which can be extended in other non-cyanobacterial species. In addition, an online DNA design portal has also been established to increase the accessibility and usability of CyanoGate which is currently maintained by Edinburgh Genome Foundry.

10.6

Engineering Cyanobacteria for Enhancing Abiotic Stress Tolerance

Abiotic stresses affect cyanobacterial growth either by imposing high light intensities or temperatures that disturb their natural circadian rhythm and photosynthetic apparatus, or heavy salinization of groundwater along with heavy metals may

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severely affect their growth and metabolism (Marques et al. 2016; Saraf et al. 2017). Being capable of adapting to diverse ecological niches and the presence of a smaller genome, cyanobacteria offer a suitable model to modify their metabolic and signalling pathways for arming them against different environmental stresses (Luan and Lu 2018). Recent findings have indicated that physiological regulatory networks significantly upregulate the transcription of various downstream stress-responsive genes which in turn activate the protective mechanisms by efficiently maintaining ion/osmotic homeostasis of cyanobacterial cells under environmental fluctuations (Rai et al. 2019). So, efforts are needed to tailor innate immune response systems using synthetic biology tools to enhance their survival under climate extremes. In this context, the engineering of GroESL system-dependent heat shock proteins (HSPs) offers a unique possibility to prevent protein aggregation and simultaneously improve the proper folding of stress-responsive proteins. A body of literature has suggested that the engineering of native HSPs of groESL has improved the growth of Anabaena PCC 7120 at 42  C and also under 50 mM salinity stress (Nakamoto et al. 2000; Luan and Lu 2018). Similarly, overexpression of HSP-dependent clpB1 gene enhanced re-solubilization and disaggregation of target protein, thus enabling the survival of Synechococcus sp. PCC 7942 at 48–50  C (Eriksson and Clarke 1996; Chaurasia and Apte 2009). Su et al. (2017) engineered and overexpressed HSP encoding gene hspA which improved the growth of Synechococcus PCC 7942 not only under high-temperature conditions but also under salinity stress. Manipulation of heterologous endogenous regulators and their subsequent integration can revitalize the regulatory and signalling networks leading to improved growth and adaptation of cyanobacterial cells to specific stresses (Aikawa et al. 2015). Modifying Synechocystis sp. PCC 6803 by integrating engineered group II sigma factor (SigB) resulted in improved growth of Synechocystis under high-temperature stress and butanol production (Kaczmarzyk et al. 2014). Similarly, Anabaena PCC 7120 overexpressing DNA-binding protein (all3940), all1122, alr0750 and phytochelatin synthase (alr0975) have shown multiple stress tolerance including UV, salinity, heavy metals and desiccation due to differential expression of their proteome pattern (Narayan et al. 2010; Chaurasia et al. 2017; Sen et al. 2019). Researchers have also exploited Na+/H+ antiporter encoding nhaP gene from Aphanothece halophytica to enhance the growth of engineered cyanobacterial strain Synechococcus sp. PCC 7942 under 0.5 M NaCl (Waditee-Sirisattha et al. 2012). Metabolic engineering for substantial and improved production of stress-responsive metabolites such as proline or glycine betaine could be a promising approach to overcome abiotic stress-induced oxidative damages and Waditee-Sirisattha et al. (2012) have successfully engineered freshwater cyanobacteria Anabaena PCC 7120 and Anabaena doliolum by modulating glycine betaine synthesis pathway to improve their growth under salinity stress. In addition, they also modified serine hydroxymethyl transferase (SHMT), an enzyme which catalyzes the conversion of serine to glycine for nucleic acid biosynthesis and other macromolecules, and integrated successfully in model cyanobacteria Synechococcus sp. PCC 7942 to improve their growth under salinity stress up to twofold (Waditee-Sirisattha et al. 2017).

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Frontline Approaches for Modifying Cyanobacterial Genome

Significant progress has been made in recent years and various genome-based approaches can also be exploited in developing more synthetic biology tools for cyanobacteria. The development of suitable phenotyping methods is of utmost requirement to accelerate cyanobacterial engineering. Screening methods such as single-cell phenotyping, high-throughput droplet phenotyping method and their subsequent modifications in the future can enhance the screening of RBS-based promoters in the recombinant libraries. Flux balance analysis (FBA), a mathematical algorithm used for characterizing the metabolic and signalling networks in different microorganisms (Orth et al. 2010), helps to analyze genome-scale reconstructions of several organisms (Qian et al. 2017a). Modifying FBA and related methods can be efficiently used to create gene knock-outs, overexpression constructs to increase the physiological ability of an organism to improve growth and sustainable bioproduction under climate extremes. Efforts have been directed to refine the existing genome-based models or construct the new ones with high fidelity, wider application and increased accuracy using computer-based algorithms. Genomebased models such as Optgene, OptKnock and OptORF and minimization of metabolic adjustment (MOMA) have been refined using in silico-based algorithms to predict target insertions and deletions controlling the synthesis of essential metabolites (Shabestary and Hudson 2016; Lin et al. 2017). Therefore, developing more in silico-based algorithms with wider applicability in different cyanobacterial strains will boost the metabolic engineering strategies for their possible biotechnological applications.

10.8

Conclusion and Future Direction

Cyanobacteria are arguably the most promising microbial platform for sustainable biotechnologies, still unravelling their full potential demands application of cuttingedge synthetic biology techniques. Significant efforts have been made to characterize genetic tools such as promoters, RBS, riboswitches, sRNA and CRISPR/Cas systems for developing robust expression libraries in heterologous organisms such as E. coli and yeast, while cyanobacteria still lag behind in the optimization of these synthetic biology tools for improving the efficiency of genetic engineering and understanding its complex regulatory networks. In view of that, this chapter provides significant insights into recent developments made in the synthetic biology tools and their application for engineering cyanobacteria to withstand environmental perturbation during their outdoor cultivation as well as to increase the bioproduction of essential metabolites for the biotechnological and agricultural endeavour. Successful utilization of cyanobacteria for industrial/agricultural applications requires the development of genetically modified strains that are more compatible with their outdoor cultivation. The application of the CRISPR/Cas tool has opened the

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possibility of using synthetic biology tools for engineering cyanobacterial species endowed with enhanced tolerance to abiotic stresses. Acknowledgements L.C. Rai thanks the Indian Council of Agricultural Research-National Bureau of Agriculturally Important Microorganisms (ICAR-NBAIM), SERB Govt of India and NASI Senior Scientist Platinum Jubilee Fellowship for financial support. Krishna Kumar Rai is thankful to NASI for Research associateship (RA), Ruchi Rai to DST-New Delhi for Women Scientist Scheme A (WOSA), and Shilpi Singh to DS Kothari, UGC, New Delhi for Post-Doctoral Fellowship (DSKPDF).

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Tan B, Ng CM, Nshimyimana JP, Loh LL, Gin KYH, Thompson JR (2015) Next-generation sequencing (NGS) for assessment of microbial water quality: current progress, challenges, and future opportunities. Front Microbiol 6:1027 Taton A, Ma AT, Ota M, Golden SS, Golden JW (2017) NOT gate genetic circuits to control gene expression in cyanobacteria. ACS Synth Biol 6(12):2175–2182 Thiel K, Mulaku E, Dandapani H, Nagy C, Aro EM, Kallio P (2018) Translation efficiency of heterologous proteins is significantly affected by the genetic context of RBS sequences in engineered cyanobacterium Synechocystis sp. PCC 6803. Microb Cell Factories 17(1):34 Ueno K, Sakai Y, Shono C, Sakamoto I, Tsukakoshi K, Hihara Y, Sode K, Ikebukuro K (2017) Applying a riboregulator as a new chromosomal gene regulation tool for higher glycogen production in Synechocystis sp. PCC 6803. Appl Microbiol Biotechnol 101(23–24):8465–8474 Ungerer J, Pakrasi HB (2016) Cpf1 is a versatile tool for CRISPR genome editing across diverse species of cyanobacteria. Sci Rep 6:39681 Vasudevan R, Gale GA, Schiavon AA, Puzorjov A, Malin J, Gillespie MD, Vavitsas K, Lea-Smith DJ (2019) CyanoGate: A modular cloning suite for engineering cyanobacteria based on the plant MoClo syntax. Plant Physiol 180(1):39–55 Veetil VP, Angermayr SA, Hellingwerf KJ (2017) Ethylene production with engineered Synechocystis sp PCC 6803 strains. Microb Cell Factories 16(1):34 Vijay D, Akhtar MK, Hess WR (2019) Genetic and metabolic advances in the engineering of cyanobacteria. Curr Opin Biotechnol 59:150–156 Waditee-Sirisattha R, Kageyama H, Tanaka Y, Fukaya M, Takabe T (2017) Overexpression of halophilic serine hydroxymethyltransferase in fresh water cyanobacterium Synechococcus elongatus PCC7942 results in increased enzyme activities of serine biosynthetic pathways and enhanced salinity tolerance. Arch Microbiol 199(1):29–35 Waditee-Sirisattha R, Singh M, Kageyama H, Sittipol D, Rai AK, Takabe T (2012) Anabaena sp. PCC7120 transformed with glycine methylation genes from Aphanothece halophytica synthesized glycine betaine showing increased tolerance to salt. Arch Microbiol 194(11): 909–914 Wang B, Eckert C, Maness PC, Yu J (2017) A genetic toolbox for modulating the expression of heterologous genes in the cyanobacterium Synechocystis sp. PCC 6803. ACS Synth Biol 7(1): 276–286 Wendt KE, Ungerer J, Cobb RE, Zhao H, Pakrasi HB (2016) CRISPR/Cas9 mediated targeted mutagenesis of the fast-growing cyanobacterium Synechococcus elongatus UTEX 2973. Microb Cell Factories 15(1):115 Xiao Q, Min T, Ma S, Hu L, Chen H, Lu D (2018) Intracellular generation of single-strand template increases the knock-in efficiency by combining CRISPR/Cas9 with AAV. Mol Gen Genomics 293(4):1051–1060 Yadav S, Rai R, Shrivastava AK, Singh PK, Sen S, Chatterjee A, Rai S, Singh S, Rai LC (2018) Cyanobacterial biodiversity and biotechnology: a promising approach for crop improvement. In: Crop improvement through microbial biotechnology. Elsevier, pp 195–219 Yao L, Cengic I, Anfelt J, Hudson EP (2015) Multiple gene repression in cyanobacteria using CRISPRi. ACS Synth Biol 5(3):207–212 Yoshikawa K, Aikawa S, Kojima Y, Toya Y, Furusawa C, Kondo A, Shimizu H (2015) Construction of a genome-scale metabolic model of Arthrospira platensis NIES-39 and metabolic design for cyanobacterial bioproduction. PLoS One 10(12):e0144430 Zess EK, Begemann MB, Pfleger BF (2016) Construction of new synthetic biology tools for the control of gene expression in the cyanobacterium Synechococcus sp. strain PCC 7002. Biotechnol Bioeng 113(2):424–432 Zhou J, Zhu T, Cai Z, Li Y (2016) From cyanochemicals to cyanofactories: a review and perspective. Microb Cell Factories 15(1):2

The Potential of Rhizobacteria for Plant Growth and Stress Adaptation

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Gustavo Ravelo-Ortega and José López-Bucio

Abstract

Plants host a very rich microbiome comprising fungi, bacteria, and protozoa. Bacteria proliferate inside tissues or around roots, where carbon-rich compounds exert positive chemotaxis. Many physiological functions in crops are related to symbiotic events with Gram-positive or Gram-negative bacteria, which influence growth, development, nutrition, and immunity and fine-tune root tropisms. This potentiates the exploration of the substrate and may confer stress tolerance. The production of secondary metabolites and volatile compounds has been thoroughly investigated in Gram-positive bacteria in recent years, and a few of these info-chemicals increase the endogenous auxin levels and/or response, whereas Gram-negative species releases quorum-sensing signals of the N-acylhomoserine type that are recognized by roots to strengthen root branching and immunity. This chapter reviews the contributions of rhizobacteria to enhance crop fitness in the field to make agriculture safer and more sustainable and highlights a few examples of how cross-kingdom signaling influences root behavior.

11.1

Introduction

Agriculture is the primary economic activity enabling food supply worldwide. Starting from the so-called “green revolution” driven by Dr. Norman Borlaug and his coworkers, through the development of crops more efficient to take up nutrients and water and more resistant to environmental challenges along with industrial

G. Ravelo-Ortega · J. López-Bucio (*) Instituto de Investigaciones Químico-Biológicas, Universidad Michoacana de San Nicolás de Hidalgo, Morelia, Michoacán, Mexico e-mail: [email protected] # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2022 U. B. Singh et al. (eds.), Re-visiting the Rhizosphere Eco-system for Agricultural Sustainability, Rhizosphere Biology, https://doi.org/10.1007/978-981-19-4101-6_11

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production of fertilizers, now we may have access to fruits and fiber to satisfy world’s demand in the few following years. Nevertheless, continuous population growth has led to the undesirable situation of the opening of natural ecosystems to agriculture, despite these lands may not be adequate to support plantations in the long term (Gomiero 2016). Another challenging trend is that the excessive use of agrochemicals has led to soil salinity, water contamination, and environmental risks (Atafar et al. 2008). Recent approaches to make agriculture more sustainable take advantage of the mutualistic relationships that plants establish with microorganisms, mainly bacteria and fungi. The root microbiome contains a great diversity of rhizobacteria that positively impact plant growth, help in phytoremediation, nutrient solubilization, or prevent diseases (Alori et al. 2017; Köhl et al. 2019; Jiang and Fan 2008). Besides, through chemical communication with root cells, rhizobacteria amplify host responses associated with the tolerance to biotic and abiotic challenges (Bano and Muqarab 2017; Chiappero et al. 2019). The establishment of rhizobacterial populations is promoted by root exudates, which are mainly constituted of carbohydrates, amino acids, organic acids, and secondary metabolites. Changes in the chemical composition of the rhizosphere influence the microbiome and, consequently, modify the overall plant adaptive responses (Sasse et al. 2018). The competition of soil microorganisms for space along roots drives the association between different bacterial taxa (Philippot et al. 2013). Consortia establishment allows the integration of diverse traits related to the growth of the host and health maintenance (Kumar et al. 2016). Recent studies have identified compatible rhizobacteria for consortia formulation and farming practices. Here, we present an overview of the rhizobacterial mechanisms that benefit crops and how these can be modulated when bacteria coexist within plant roots.

11.2

Rhizobacterial Functions in Plant Growth and Development

Plant developmental processes such as embryogenesis, germination, growth, flowering, and reproduction are regulated by a wide range of compounds named phytohormones, many of which can be produced by rhizobacteria. Indole-3-acetic acid (IAA) is the most widely distributed auxin in plants and microorganisms that stimulates root growth and organogenesis (Perrot-Rechenmann 2010). Through changes in the configuration of the root system, bacteria improve soil exploration and, therefore, nutrient uptake (Fig. 11.1). Pseudomonas, Bradyrhizobium, Streptomyces, Azospirillum, Sphingomonas, and Acinetobacter species that actively produce IAA constitute important options to enhance crop performance (Chouyia et al. 2020; Hashmi et al. 2019; Ijaz et al. 2019; Kumawat et al. 2019; Molina-Romero et al. 2017).

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Fig. 11.1 Plant growth enhancement by rhizobacterial species. Soil bacteria can improve plant growth and development contributing to P solubilization by the production of chelating substances and organic acids. The enzymatic machinery of some rhizobacteria allows to convert the atmospheric nitrogen into assimilable N forms for plants. Phytohormones produced by rhizobacteria reconfigure the root system architecture in a way that improves its ability to explore the soil and therefore boosts the uptake of nutrients

11.3

Enhanced Nutrient Uptake

Plants rely on an adequate supply of minerals for growth and development. When a given soil lacks any macro- or micronutrients, various physiological processes are altered, decreasing their productivity. Phosphorus (P) and nitrogen (N) are the most limiting elements for the success of crops due to their structural, metabolic, and signaling functions. Most nutrients should be supplied in their ionic forms as part of chemical fertilizers or as part of organic amendments that farmers use to warrant high productivity (Maathuis 2009). Phosphorus commonly remains in the soil as insoluble phosphate complexes, not easily available for uptake by the root system. The production of organic acids, chelating substances, and enzymes from rhizobacterial species promotes solubilization of organic and inorganic P forms,

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which can be taken up by root hairs and lateral roots (Alori et al. 2017). Such ability to solubilize P is an interesting trait of bacteria that increases the growth and yield parameters in tomatoes and maize (Bradáčová et al. 2019, 2020) and supports growth in P-deficient soils (Bradáčová et al. 2019). Noteworthy, a mixture of Pseudomonas sp., Burkholderia sp., Enterobacter sp., and Serratia sp. improved both the available P content in soil and its uptake in aloe plants (Gupta et al. 2012). Rhizobacteria may support N reduction to form nitrate (NO3 ) and ammonium (NH4+) for plant nutrition. Particularly, the Rhizobium genus stimulates the growth of legumes through N fixation in root nodules (Vargas et al. 2017). The mineralization of organic matter contributes to enriching the pool of available N in the soil by the activity of lytic enzymes from saprophytic bacteria and fungi (Geisseler et al. 2010). Soybean and common bean seeds inoculated with Bradyrhizobium sp. and co-inoculated with Azospirillum sp. generated the same yield under N deficiency conditions as in fertilized soils. This consortium is an example of alternatives less expensive for farmers to support productivity (Hungria et al. 2013). Integration of rhizobia species including Bradyrhizobium sp., R. leguminosarum, and Sinorhizobium meliloti synergistically increased the nodule number, biomass, and the N uptake in soybean and pigeon pea (Kumar et al. 2016; Kumawat et al. 2019; Pandey and Maheshwari 2007). Plant nutrition also demands several trace elements that play critical roles in redox reactions and function as cofactors of several enzymes such as RNA polymerase, cytochromes, and superoxide dismutase (Nagajyoti et al. 2010). Bacteria can help plants, either by solubilizing these micronutrients through acidifying the soil or by releasing siderophores that act as metal chelators (Abbaszadeh-Dahaji et al. 2016; Scavino and Pedraza 2013). Wheat plants whose seeds were treated with Bacillus sp., Providencia sp., and Brevundimonas sp. mixtures showed better content of Fe, Zn, Cu, and Mn (Rana et al. 2012). Another triple consortium (B. megaterium, Arthrobacter chlorophenolicus, and Enterobacter sp.) applied to wheat seeds increased the content of microelements in the harvested grains (Kumar et al. 2014).

11.4

Tolerance to Abiotic Stress

Soil pollution caused by natural or anthropogenic factors and extreme weather conditions are detrimental to agriculture. Heavy metals, salinity, drought, and drastic temperature fluctuations are the principal abiotic stresses that negatively impact crop growth and productivity (Farooq et al. 2012; Nagajyoti et al. 2010; Parihar et al. 2015; Mathur and Jajoo 2014). Physiological consequences of abiotic stress reside in overproduction of reactive oxygen species (ROS) and the emission of the gaseous phytohormone ethylene (Kumar and Verma 2018). ROS include free radicals that act as messengers in cell signaling through the so-called oxidative stress response. Disturbed ROS homeostasis compromises cell integrity and may cause cell death (Sharma et al. 2012). ROS affect membrane stability via lipoperoxidation and damage proteins and nucleic acids, and thus plants employ scavenging enzymes such as peroxidase, superoxide dismutase, catalase, polyphenol oxidase, and

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Fig. 11.2 Rhizobacteria mitigate abiotic and biotic stress in plants. Arrows represent positive or negative regulation. Soil bacteria produce numerous enzymes and compounds that directly reduce the soil pollution caused by heavy metals and eliminate the soilborne phytopathogens (brown arrows). The induced systemic tolerance and the induced systemic resistance in plants, which involve components that attenuate the impact of abiotic and biotic stresses, can be activated by rhizobacteria (grey arrows). ACC deaminase from bacteria can decrease ethylene overproduction triggered in plants in response to several stresses (pink arrows). Overall, growth/defense trade-offs are finely modulated in symbiotic interactions

antioxidant compounds including proline, glutathione, ascorbic acid, carotenoids, vitamins, and flavonoids to diminish the oxidative stress (Mehla et al. 2017). Also, as part of adaptive strategies, plants maintain a precise balance in the amount of ethylene synthesized from aminocyclopropane-1-carboxylic acid (AAC) through ACC deaminase enzyme activity that degrades ACC to α-ketobutyrate and ammonia (Shi et al. 2012; Singh et al. 2015). A practical and eco-friendly strategy to mitigate these nonbiological stresses is the use of probiotic microbes (Fig. 11.2). Rhizobacteria can restore soil fertility by eliminating contaminants and inducing morphological, physiological, and gene expression changes in plants to improve their resistance through a mechanism

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termed induced systemic tolerance (IST) (Etesami and Maheshwari 2018). Indeed, rhizobacteria provide a combination of different and potential properties that reinforce the plant tolerance to abiotic stresses (Rajput et al. 2018; Saikia et al. 2018; Silambarasan et al. 2019).

11.4.1 Heavy Metals Fe, Zn, Mn, Mo, Cu, and Ni are heavy metals considered micronutrients for plants in low micromolar or nanomolar concentrations. However, higher concentrations of these minerals (i.e., millimolar range) or other nonessential metals led to adverse effects on germination and shoot and root development not only by oxidative damage, but also by causing enzymatic dysfunction, chlorosis, and senescence (Nagajyoti et al. 2010). Heavy metal pollution in soils represents a problem for agriculture and human health, and its origin can be natural (i.e., volcanic eruptions and rocks) or industrial (mining and smelting) (Alloway 2013; Ma et al. 2019; Wei et al. 2018). Long-term application of fertilizers and pesticides may also pollute the soils with heavy metals (Atafar et al. 2008). The use of microorganisms is one of the cheapest and most ecological alternatives for the restoration of contaminated soils. Certain bacteria can precipitate, methylate, reduce, oxidize, and chelate heavy metals to attenuate their toxicity (Jiang and Fan 2008; Ojuederie and Babalola 2017). Phosphate organic compounds, as well as siderophores, can interact and bind heavy metals. Shilev et al. (2020) isolated a bacterial consortium (Pseudomonas spp. and Bacillus sp.) tolerant to heavy metals and inoculated it to spinach seeds in soils contaminated with Pb, Zn, and Cd. The consortium showed the capacity to precipitate or immobilize heavy metals forming insoluble complexes and at the same time increased phosphate solubilization and siderophore production. Plants treated with the bacterial mixture had less accumulation of heavy metals in leaves, stems, and roots and sustained remarkable growth. Another bacterial consortium supported the Pb and Cd immobilization, increasing the phosphate solubilization (Yuan et al. 2017). Through interaction with their functional groups, exopolysaccharides from bacteria also retain various heavy metals (Morillo Pérez et al. 2008). Phosphate solubilizing activity, siderophore, and exopolysaccharide production are traits of B. megaterium and Pantoea agglomerans that enhance the growth of mung bean plants in soils polluted with Al reducing its concentration in tissues (Silambarasan et al. 2019). Plants possess mechanisms to counteract the toxicity of heavy metals. For instance, compounds from root exudates such as organic acids, carbohydrates, and siderophores retain toxic elements by chelation, avoiding their absorption by crops (Nagajyoti et al. 2010). These mechanisms can be over-induced by rhizobacteria, allowing the plants to continue growing, even at high concentrations of heavy metals (Silambarasan et al. 2019).

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11.4.2 Salinity Salinization is a severe problem for plant development that has spread to 20% of irrigated lands. Unlike halophytes, most crops exhibit physiological problems when grown in soils with moderate or high salt concentrations (Abogadallah 2010; Farooq et al. 2015). Saline stress increases the Na+ and Cl levels in the cytoplasm and chloroplasts, provoking an osmotic imbalance that stimulates ROS and ethylene overproduction and affects photosynthesis and plant growth (Amjad et al. 2014; Dar et al. 2017; Farooq et al. 2015). Cellular responses to salinity imply the production of osmoregulatory solutes, increased antioxidant activity, and improved selectivity of ions (Ahanger et al. 2017; Amjad et al. 2014). Highly efficient mechanisms are employed by rhizobacteria isolated from halophytes to improve the host adaptation to saline soils (Abbas et al. 2019; Jiménez-Vázquez et al. 2020). These microbes regulate the rhizosphere osmolality and promote adaptation through counteracting saline shock (Bharti et al. 2016; Sarma et al. 2012). Halotolerant rhizobacteria such as Achromobacter sp., Serratia sp., and Enterobacter sp., which presented ACC deaminase activity and IAA production, were found to increase the length of the shoot and root system in avocado plants exposed to saline stress conditions. The consortium intensified the superoxide dismutase activity and diminished lipoperoxidation (Barra et al. 2017). Halotolerant Aeromonas spp. mixture protected wheat plants from saline stress improving the root and leaf biomass and increasing the grain yield under half chemical fertilization (Rajput et al. 2018).

11.4.3 Drought Comparable to salt toxicity, drought increases osmotic stress. The main physiological processes altered by drought are photosynthesis and the uptake and transport of nutrients (Farooq et al. 2012). Therefore, the germination, growth, and development of plants are drastically disrupted under this adverse condition (Asrar and Elhindi 2011; Liu et al. 2011; Samarah and Alqudah 2011). Under drought, plants raise the synthesis of abscisic acid, a phytohormone that induces stomatal closure and prevents water loss through transpiration (Tombesi et al. 2015). Rhizobacteria may support plant growth in water-deficient conditions via decreasing stomatal aperture and reducing ethylene levels (Chiappero et al. 2019; Cho et al. 2008; Mayak et al. 2004). Rhizobacterial consortia alleviated the growth repression of common bean and mung bean triggered by drought stress (Figueiredo et al. 2008; Silambarasan et al. 2019). Crops exposed to drought and grown under pretreatments with bacteria showed more superoxide dismutase, peroxidase, and catalase activity (Barra et al. 2017; Kohler et al. 2008). The mixture of Ochrobactrum sp., Pseudomonas sp., and Bacillus sp. had a synergic effect on the growth of different plant species exposed to drought. Also, they reduce the ACC levels in plants (Saikia et al. 2018).

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11.4.4 Temperature Extreme temperatures either heat or cold affect crop productivity. Production of ROS, heat shock proteins, and abscisic acid and the activation of mitogen-activated protein kinases (MAPKs) are part of the signaling mechanisms triggered by heat stress (Andrási et al. 2019; Evrard et al. 2013; Guo et al. 2016; Link et al. 2002; Yu et al. 2019). Elevated temperatures impair water content, photosynthesis, and membrane stability (Liu and Huang 2000; Mathur et al. 2011; Wassie et al. 2019). Thermotolerant rhizobacteria can enhance plant mechanisms associated with tolerance to heat stress, such as the production of osmolytes, activation of antioxidant enzymes, and reduction of ethylene levels (Ali et al. 2011; Khan et al. 2020; Mukhtar et al. 2020; Sarkar et al. 2018). The foliage is very sensitive to cold stress and is one of the organs more impacted by chilling, exhibiting wilting, necrosis, chlorosis, and deformation, which affect early leaf growth and flowering (Kumar et al. 2010; Rymen et al. 2007; Yadav 2010). Acclimation to low temperatures is regulated positively by abscisic acid since mutants altered in the signaling of this phytohormone are hypersensitive to cold stress (Shi and Yang 2014). Adverse effects of cold stress can be attenuated by an overproduction of solutes such as sugars and amino acids, whose accumulation is stimulated through interaction with rhizobacteria (Ait Barka et al. 2006; Fernandez et al. 2012; Mishra et al. 2011). Tomato plants grown in soil inoculated with B. cereus, B. subtilis, and Serratia sp. were exposed to cold stress and showed a high level of hydrogen peroxide (H2O2) than non-inoculated plants. After days, the consortium moderated the oxidative stress caused by low temperatures mainly through the activation of superoxide dismutase and peroxidase activities. Besides, rhizobacteria increased the production of osmoprotectants such as proline and sugars. These effects helped to reach almost 100% plant survival (Wang et al. 2016). Kakar et al. (2016) applied a combination of Bacillus sp. and Brevibacillus sp. in rice seedlings and then applied cold stress treatment. The bacteria improved cold tolerance, upregulated the activity of antioxidant enzymes, and increased the proline content of plants, stimulating their growth and survival.

11.5

Biotic Challenges

Considerable crop losses occur due to nematode, viral, bacterial, oomycete, and fungal pathogens, which cause damage at each developmental stage (Savary et al. 2019). The control of plant diseases has been possible in the last decades by applying biocides that pollute air, water, and soil, damage pollinators, and ultimately enter the food chain (Popp et al. 2013; He et al. 2016). Thus, an important goal to achieving sustainable productivity is to develop new alternatives based on understanding plantmicrobe interactions in an ecological context (Fig. 11.2). Plants manifest constitutive and inducible defenses to protect themselves from pathogens. The properties of their immune system can be further modulated by abiotic and biotic stresses (Jain et al. 2016; Miura and Tada 2014). Detailed

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information on how plant defense is mounted has been gathered in leaves, and until recently little was known about how roots react under attack. It has become evident that damaged roots unlock a protective mechanism in coordination with probiotic bacteria surrounding them that boosts the defense reaction (Berendsen et al. 2012; Hematy et al. 2009).

11.5.1 Disease Suppressive Soils Some soils have the property to suppress plant diseases because their microbiomes inhibit the spread of phytopathogens. On the other hand, the so-called conducive soils favor the incidence of plant diseases (Schlatter et al. 2017). Abiotic factors and certain farming practices can influence the growth of microorganisms related to the balance required for plants to survive and thrive (Jansson and Hofmockel 2020; Mehta et al. 2014). Continuous cropping is a practice that diminishes rhizobacterial diversity, generating a higher vulnerability to the root rot disease (Tan et al. 2017). In contrast, monocropping systems triggered the reduction of take-all disease, a phenomenon linked to the rising of P. fluorescens (Sanguin et al. 2009). The release of root exudates attracts specific groups of bacteria, causing changes in the soil microbial composition that reinforces defensive barriers (Berendsen et al. 2012). Proteobacteria, Firmicutes, Acidobacteria, and Actinobacteria strains predominate in the bacterial community of suppressive soils associated with tolerance to distinct crop diseases (Cha et al. 2016; Kyselkova et al. 2009; Sanguin et al. 2009). Mendes et al. (2011) dissected the rhizobacterial microbiome of sugar beet cultivated in suppressive soils of damping-off disease, concluding that the bacterial taxa contribute to disease mitigation. Seven rhizobacterial strains delayed the Fusarium verticillioides mycelial growth on maize seeds and decreased the blight disease incidence in seedlings. Each bacterial strain had a biocontrol effect on spreading the fungus and disease incidence, but not to the same degree as the consortium did (Niu et al. 2017). Other rhizobacteria showed a synergistic biocontrol on the blast disease in rice and collar rot disease in betelvine (Lucas et al. 2009; Singh et al. 2003). This protective capacity could persist for more than one season (Zhang et al. 2019). Therefore, multiple mechanisms depending on the composition of the microbial consortia account for the natural root antagonism to soilborne pathogens.

11.5.2 Fighting Plant Diseases The production of antibiotics such as 2,4-diacetylphloroglucinol (2,4-DAPG), phenazine-1-carboxylic acid, pyrrolnitrin, oomycin, aerugine, and kanosamine is an important mechanism used by rhizobacteria to suppress the growth of phytopathogens (Kenawy et al. 2019). These compounds damage cell membranes, interfere with the electron transport chain, and affect enzymatic activity (Janiak and Milewski 2001; Raaijmakers et al. 2009; Troppens et al. 2013). Santhanam et al. (2019) evaluated biofilm development during the colonization of tobacco roots by

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Bacillus sp., Pseudomonas sp., and Arthrobacter sp. This consortium increased plant survival against the sudden wilt disease, and one of the factors associated with the resistance was the production of surfactin, an antifungal compound. A single antibiotic can control diverse phytopathogens; for example, 2,4-DAPG, produced by several Pseudomonas strains, suppressed take-all, root rot, and damping-off fungal diseases and crown gall caused by Agrobacterium tumefaciens (Weller et al. 2007). Cell wall degrading enzymes can be secreted by rhizobacteria that affect fungal phytopathogens. Chitinase and glucanase production is one of the desirable determinants to select rhizobacteria for biocontrol (Pliego et al. 2011). In this manner, the attenuation of F. oxysporum in maize was made possible, and at the same time plant growth and yield increases were obtained upon applying a quadruple bacterial inoculum composed of B. megaterium, P. aeruginosa, Serratia sp., and P. fluorescens (Akhtar et al. 2018). Micronutrient availability is an ecological determinant for plant-microbe interactions. Under deficiency of Fe, an essential micronutrient, specific bacteria produce and secrete siderophores to chelate the available iron, rendering it unavailable for phytopathogens (Kramer et al. 2020). Treatments of Pseudomonas sp. or its siderophores protected plants against Gaeumannomyces graminis and F. oxysporum (Kloepper et al. 1980). Besides, some consortia had suppressive effects related to the activity of siderophores (Akhtar et al. 2018; Estevez de Jensen et al. 2002; Santhanam et al. 2019).

11.5.3 Plant Defensive Reactions The plant immune system is reinforced by gene expression related to lytic enzymes and the production of antimicrobial compounds (Jain et al. 2016). Two main pathways control the defense reactions, the first involves systemic acquired resistance (SAR), stimulated after an attack of pathogens and dependent on the phytohormone salicylic acid. SAR induces pathogenesis-related (PR) genes, and it is initially manifested in the damaged site but later spreads systemically to distant tissues (Klessig et al. 2018). In the second pathway, the so-called induced systemic resistance (ISR) involves plant interactions with nonpathogenic rhizobacteria, which promote defense-related gene expression through signaling of the phytohormones ethylene and jasmonic acid. ISR has been reported to occur in the aerial and root system and also in leaves, keeping the plant defense machinery ready and alert to respond quickly to single and multiple biotic stimuli (Pieterse et al. 2014). Berendsen et al. (2018) isolated three bacterial strains from the Arabidopsis thaliana rhizosphere, which prevailed during foliage infection caused by the oomycete Hyaloperonospora arabidopsidis. The plants grown in soil previously inoculated with these rhizobacteria showed less incidence of the oomycete in leaves. Besides, a combination of rhizobacteria and plant growth-promoting fungi (PGPF) protected cucumber plants against F. oxysporum infection in stems, enhancing the expression of genes encoding chitinases, glucanases, and enzymes involved in the

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synthesis of antifungal compounds (Alizadeh et al. 2013). Peroxidase is another defense component of plants that limits the pathogen spread as it mediates the establishment of physical barriers such as lignin and suberin in cells (Passardi et al. 2005). Adjusting the levels of reactive oxygen species, both peroxidase and superoxide dismutase, can create a toxic environment for pathogens in plant cells (Torres et al. 2006). Bacillus spp. diminished the bacterial and fungal infection in tomato and pepper apparently by induction of the peroxidase and superoxide dismutase activity (Jetiyanon 2007). The plant phenylpropanoid pathway directs the production of phenolic compounds with antimicrobial properties. Phenylalanine ammonia-lyase converts L-phenylalanine into trans-cinnamic acid, a precursor for the synthesis of phenolics (Cheynier et al. 2013). Indeed, polyphenol oxidase oxidizes phenols to generate quinones, which also inhibit phytopathogen growth (Jukanti 2017). Pseudomonas sp., Rhizobium sp., and Trichoderma sp. reduced the mortality in chickpea plants infected by Sclerotium rolfsii. The triple microbial consortium enhanced the gene expression of peroxidase and superoxide dismutase and increased phenylalanine ammonia-lyase, polyphenol oxidase activity, and lignin deposition (Singh et al. 2013).

11.5.4 Quorum-Sensing-Mediated Antagonistic Activity Colonization of roots, either by beneficial microorganisms or by plant pathogens, initiates a complex interrelationship where root exudates and mineral nutrients play an essential role. The formation of biofilms mainly composed of bacteria is a biological barrier that extends beyond the root epidermis. This process is under the control of a cell-to-cell chemical communication program termed quorum sensing (QS). In Gram-negative bacteria, QS controls the transcription of genes by producing small molecules, mainly the N-acyl-L-homoserine lactones (AHL) (Dwivedi et al. 2017). These compounds have strong activity not only in bacteria but also in roots, which suggests that they modulate the inter-kingdom plant-bacteria language (Ortíz-Castro et al. 2008). Mutants of P. chlororaphis deficient in QS regulation lost their ability to inhibit the growth of plant pathogens. These variants exhibited low expression of phzA/ prnA genes related to the production of two broad-spectrum antibiotics phenazine-1carboxylic acid and pyrrolnitrin. AHL supplements induced the prnA expression, indicating that the QS compounds directly trigger pyrrolnitrin synthesis (Selin et al. 2012; Shah et al. 2020). Kim et al. (2017) concluded that the QS in Chromobacterium sp. supports its capacity to suppress fungal diseases in plants since the mutation of the gene encoding homoserine lactone synthetase reduced its chitinolytic activity. Other rhizobacterial enzymes attenuated the virulence of phytopathogenic bacteria by degrading QS molecules. For instance, Actinobacteria releases lactonases, which degrade AHLs in Pectobacterium carotovorum and affect its virulence (Vesuna and Nerurkar 2020). The interaction between bacterial

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communities also upregulated or downregulated the production of siderophores via QS signals (Shah et al. 2020; Stintzi et al. 1998; Whiteley et al. 1999).

11.6

Perspectives

Plants and microorganisms have developed inter-kingdom relations, which have been gaining special attention in agriculture since they improve crop yields and may reduce fertilization and pest control costs. The combination of selected traits from two or more bacteria further intensifies the probiotic effects on crops. Competition for energy and nutrient sources from exudates has led rhizobacteria to influence the host defense responses against bacteria and fungi that could be a threat. Therefore, it is crucial to identify and understand the mechanisms that define rhizobacteria compatibility and antagonism to develop successful inoculants. Exploration of natural ecosystems has proven to be a valuable strategy to identify novel traits in both bacteria and plants useful to resist stress. The search for halophyte bacteria in a largely untouched sink hole termed the “Poza Salada,” located in the Chihuahua Desert, enabled the identification of a group of plant beneficial bacteria living in association with roots of well-adapted plant species, which grow healthy despite the very high salt concentrations. Three bacterial isolates typified molecularly as Bacillus sp., P. lini, and Achromobacter sp. promoted the growth of A. thaliana, Cucumis sativus, and Citrullus lanatus in vitro and in soil under standard and saline growth conditions (Jiménez-Vázquez et al. 2020; PalacioRodríguez et al. 2017). Noteworthy, Achromobacter sp. interfered with the root gravity response and caused the formation of waves and circles called coils, which primed roots for enhanced branching through the proliferation of lateral roots (Jiménez-Vázquez et al. 2020). The mechanisms underlying the beneficial properties of halophytes to plants are far from being understood; however, their protection from salinity in different plant species opens new avenues for agriculture. Regardless of the plant growth-promoting traits that rhizobacteria have in their natural niche, their survival should be tested under different environmental conditions to warrant their prevalence on crops. Generating more knowledge about the ways rhizobacteria interact with plants will facilitate access to biological tools for more productive and sustainable agriculture.

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Mycoremediation: An Emerging Technology for Mitigating Environmental Contaminants

12

Manisha Mishra and Deepa Srivastava

Abstract

Mycoremediation is a technique that transmutes toxic, recalcitrant pollutants into environmentally safe products by organic treatments. It is a green method for cleaning up polluted sites. Because of a breakthrough in technology, exceedingly harmful contaminants are persistently released into the environment via industries. Polycyclic aromatic hydrocarbons (PAHs), heavy metals, polychlorinated, and pharmaceutical compounds (PhC) are mutagenic. They are freed by petroleum refineries, textile mills, and vehicle exhaust. Human exposure has risen because of their rampant use in certain industrial, agricultural, and domestic fields. Recently, there has been a growing ecological and global public health concern accompanying environmental contamination. The traditional methods applied to remove them pose risk to the ecosystem. Remediation of polluted sites has become a center of attention within society because of accelerating public awareness. The theory of mycoremediation has come up from the chief role of fungi within the ecosystem, which is to decompose. Nonetheless, the dominating biomass in soil are fungi, which still have not been exploited aptly for mycoremediation. Microfungi and macrofungi both contribute to the feasibility of mycoremediation. Their wealthy enzyme compositions assist the process. The objective of this chapter is to review the role of contaminants on the environment as well as to focus on the part of fungi in eliminating them. We have discussed in detail the various works and the contemporary advancements; futuristic omics approaches that are in the midst of progress.

M. Mishra · D. Srivastava (*) Department of Botany, DDU Gorakhpur University, Gorakhpur, Uttar Pradesh, India # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2022 U. B. Singh et al. (eds.), Re-visiting the Rhizosphere Eco-system for Agricultural Sustainability, Rhizosphere Biology, https://doi.org/10.1007/978-981-19-4101-6_12

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Introduction

The industrial revolution is one of the noteworthy incidents in society. It commenced in Britain around the eighteenth century and is still ongoing. It altered our civilization from an agricultural unit to a manufacturing hub. It changed the grassroots organization and has its pros and cons. Collectively with all this came pollution! Previously, there were minor factories, but lately this business flourished into fullscale industries, and environmental pollution gained momentum. Moreover, many factories still work with age-old technologies creating huge waste. Soil contamination occurs due to the extraction of mineral ores from the earth’s crust which are essential for use as industrial raw materials. Leading complications affecting solid waste management are irrational plans and inappropriate waste collection, leading to threats such as environmental degradation and pollution of water, soil, and atmosphere. Open junkyards are a breeding place for harmful microbes and generate health hazards. Both surface and groundwater are negatively affected by this. The scarcity of genuine policies and improper enforcement protocols allowed industries to neglect the laws. Costly conventional remedial techniques and the obligations related to the use of such practices have stimulated industries to search for novel techniques. To achieve proper remedies, the scientific fraternity and technology firms are testing and discovering emerging technologies. One of these is bioremediation, which is significant nowadays. Far-reaching toxic pollutants constituted a threat to living creatures. The elimination of such contaminants is a prerequisite of present times. The physical-chemical or a union of such methods has been harnessed already. Yet factories use poisonous chemicals and generate dumping issues. The bioremediation strategy directs the use of biological microbes or fungi to do the cleanout. Methods used for remediation of toxic contaminants are rhizoremediation, phytoremediation, microbial remediation, and biosurfactants, which is a leadingedge tool. Mycoremediation in contaminated sites points at pulling out harmful pollutants. Frequently, contaminated sites can become toxin-free. The bioremediation process can be performed by the following: 1. In situ: The process is done just at the contamination site. Polluted soil or water is cured at its root source. It is a desirable method since it demands a lesser workforce. Also, it controls the spreading of contaminants to farther locations. 2. Ex situ: It requires locating contaminated material to a distant treatment spot. It is troublesome in the case of contaminated water bodies. These methods are risky as chances of contamination spreading exist. The remediation of contaminated sites has become a preference for society because of the rise in standards of living and the recognition of environmental issues. Rhizoremediation integrates plants and microbes associated with them.

12.1.1 Benefits of Bioremediation • Bioremediation is a spontaneous process. • It is carried out mostly in situ.

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It has consent of environmental panelists. Minimal tool necessity. Organic and eco-friendly method. Slight power expenditure. Budget-friendly compared to other technologies. Less alarming to the environment.

12.1.2 Drawbacks of Bioremediation • The bioremediation process is limited to the compounds that are biodegradable since all the compounds cannot be entirely degraded. • It is a tremendously specific task. • It requires an extended period than conventional methods. • If mushrooms are incorporated into the process, they can turn fatal when consumed as such since these are hyperaccumulators of toxic compounds. We can protect the deteriorating quality of our surroundings by adopting innovative technology for waste disposal and by being aware of raw materials that can alleviate pollution.

12.2

Fungi as Bioremediators

Fungi are powerful decomposers. They are responsible for breaking down most of the earth’s plants and wooden scrap into life-giving soil by breaking complex plant cell components such as cellulose and lignin into final forms (Dutta and Hyder 2017). Organic pollutants contain PAH, heavy metals, and synthetic dyes that are carcinogenic and steadily present in the surroundings. They bring about disadvantageous effects on human health. Many studies revolve around microfungi, but the focus has been shifted to macrofungi that grow abruptly on the soil. They can assemble heavy metals in their fruit bodies and can be visible in the form of mushrooms. Incorporating endemic fungi in the remediation process needs vast mycelium. Mycelia are a dense network of vegetal and thread-like hyphae. Enzymes are secreted from mycelia. An expanded hyphal network aids in the employment of toxic compounds. Their growth substrate frame filamentous fungi as superior in bioremediation to other microorganisms. Mycoremediation is a biotechnique that integrates fungi in the decontamination of altered surroundings (Kapahi and Sachdeva 2017). Enzymes secreted are extracellular and break larger molecules into smaller ones, which enter the cells for further reactions (Levasseur et al. 2014). There are diverse parts that apply mushrooms in the remediation process. Mushroom spawn is spread on contaminated sites to trap toxic compounds. Mycoremediation potential depends on the ease of accessibility of nutrient distribution in soil. Nutrients are supplemented to the soil to amplify the process (Adams et al. 2015). Introducing mushroom beds can decrease soil erosion and aid in curing

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the disrupted place. Mushrooms need ample dampness, air, shadow, and fair temperature to grow. Different mushroom species can effectively decontaminate polluted sites. Biodegradation of recalcitrant pollutants as PAHs is noticed by white-rot fungi. Combining certain strains of mushrooms can be more successful as they can together modify contaminants and hold on to the water in the soil. Befitting fungi used in soil decontamination are basidiomycetes. Two ecological groups are used in the bioremediation process (Treu and Falandysz 2017). They are as follows. Saprotrophic basidiomycetes—These are white-rot fungi and brown-rot fungi. These wood-decaying fungi use dead organic matter as a carbon source. Saprophytic fungi use their digestive enzymes to reduce harmful hydrocarbons and defoliants. The examples include Agaricus bisporus, Trametes versicolor, Pleurotus ostreatus, Irpex lacteus, Lentinula edodes, P. tuber-regium, P. pulmonaris, and Phanerochaete chrysosporium. Biotrophic basidiomycetes—They include ectomycorrhizal associations. They gain optimum nutrition by secreting enzymes that degrade the molecules present in soil organic matter. The examples are Lactarius spp., Amanita spp., Morchella spp., and Boletus spp. Fungi have great power of endurance in contrast to bacteria in fore bearing higher concentrations of pollutants. Mycelia of white-rot fungi pierce the cell cavity to release ligninolytic enzymes (Tišma et al. 2010).

12.2.1 Biosorption Mechanism Mushrooms incorporate various paths to concentrate heavy metal contaminants. Adsorption is the binding of molecules or ions upon the surface of other molecules. The surface is adsorbent and the compound accumulated is adsorbate. Bioaccumulation relates to employing living cells except for biosorption that involves lifeless biomass. Biosorption by mushrooms is productive and nontoxic as compared to the bioaccumulation process. Being a passive process, it does not require media for growth due to no damage to the biomass with contamination or cell death (Dhankhar and Hooda 2011). The solid phase is known as biosorbent. Biosorption can be listed into three types—cell surface sorption, extracellular accumulation, and intracellular accumulation. Cell surface sorption happens by interactivity between metals and functional groups present on the fungal surfaces. It focuses on adsorption and chelation properties. Intracellular accumulation can occur only in a living cell by transport across the cells (Vegliò and Beolchini 1997).

12.3

Enzymes Used by Fungi in the Remediation Process

Fungal enzymes comprise proteases, amylases, catalases, laccases, peroxidases, and so on. Polymeric compounds such as starch, cellulose, lipids, proteins, or other complex biomolecules are hydrolyzed by these enzymes. Ligninolytic enzymes secreted by white-rot fungi for lignin oxidation make up two categories—

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peroxidases, that is, lignin and manganese peroxidases (LiP, MnP), and laccases. Biodegradable extracellular enzymes are laccases and class II peroxidases. Cytochrome P450 monooxygenases and glutathione transferase are intracellular enzymes. The intracellular metabolic breakdown pathway present in mycoremediation shows affinity with secondary metabolism in fungi, especially in mycotoxin production (Chanda et al. 2016). Oxidative enzymes from fungi are prioritized because they are less substrate-specific enzymes.

12.3.1 Ligninolytic Fungal Enzymes Laccases are multicopper oxidases. Laccases can oxidize a range of phenolic and non-phenolic compounds. They function as a catalyst in industries and have bioremediation potential (Vishwanath et al. 2014). Reactive oxygen species (ROS) demolish cellular membrane that is harmful to the cell entity. Aspergillus foetidus had resilience toward Pb2+ and an inflated level of antioxidative enzymes intracellularly (Chakraborty et al. 2013). The peroxidase enzyme needs hydrogen peroxide for reactions. Fungi have innated oxidative enzyme machinery that withdraws harmful compounds. The tribromophenol level is decreased by the fungal laccase of T. versicolor (Donoso et al. 2008). Coriolus versicolor can degrade PAHs with manganese phosphate and lignin phosphate enzymes (Jang et al. 2009). Laccase of Trichoderma species decays phenanthrene (Han et al. 2004). Laccases hold a low shelf-life. Nanobiotechnology-driven studies involving laccases could be a boost.

12.3.2 Non-ligninolytic Fungal Enzymes Fungi have intracellular components that are composed of cytochrome P450 monooxygenase and glutathione transferases (Morel et al. 2013). Cytochrome P450 monooxygenase is the predecessor to degradation plans involving aromatic pollutants. Lignin-degrading enzymes do not work accordingly due to insufficient lignocellulosic substrate on contaminated soil. This limitation can be prevailed by enzymes such as cytochrome P450 monooxygenase as reported in ascomycetes (Marco-Urrea et al. 2015).

12.4

Mycoremediation of Polycyclic Aromatic Hydrocarbons

PAHs (polycyclic aromatic hydrocarbons) are emitted as a consequence of pyrolytic processes due to insufficient combustion of organic materials. They are released in industrial and other activities such as mining, combustion of gases, and smoking (Fig. 12.1). PAHs are a crowd of organic pollutants with two or more fused aromatic rings. A few examples of PAHs are naphthalene, anthracene (AC), phenanthrene, fluorene, pyrene, and chrysene. The best-known PAH is benzo[a]pyrene (BaP). Carcinogenic PAHs are prevalent in all surface soils. Exposure to benzo[a]

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anthracene, chrysene, benzo[b]fluoranthene, benzo[k]fluoranthene, and BaP is frightening. They are soluble in lipids but slightly less soluble in water. They get absorbed from the lungs, gut, and skin of mammals. Food is regarded as the leading source of human exposure to such compounds due to the generation of PAH through cooking oils or from the atmospheric accumulation of PAHs on grains, fruits, and vegetables (de Vos et al. 1990). Biodegradation methods are engaged to transform into nonhazardous forms in an ecologically sound way. Bioremediation is a crucial tool to rehabilitate the PAH-contaminated sites. The plant-microbe interaction for the disintegration of soil pollutants consequences in rhizoremediation. Hussein and Mansour (2016) reported general usage of some PAHs: 1. 2. 3. 4.

Anthracene: Dial event for food preservatives and red dye manufacturing Fluoranthene: Manufacturing of agrochemicals dyes and insulating oils Phenanthrene: Employed in resins and pesticides, plastics, and explosives Pyrenes: Manufacturing of pigment dyes and their precursors

Trichoderma lixii strain was isolated from PAH-contaminated soil and might grow on phenanthrene using it as a personal carbon source. Trichoderma species can reside in a broad spectrum of substrates by using them (Venice et al. 2020). Biodegradation of PAHs occurs under either aerobic or anaerobic conditions and could be increased by physicochemical-free treatment of contaminated soil (Cerniglia 1993). Oxygenases, peroxidases, dehydrogenases, and ligninolytic enzymes are involved in PAH degradation (Chang et al. 2002). P. ostreatus, a

Sources of P.A.Hs

Anthropogenic Sources

Natural Sources

Volcanic eruptions, Forest fires, Decaying organic matter, Seepage of petroleum

Agricultural

Domestic

Industrial

Pesticides, Herbicides, Fungicides, Inorganic or organic fertilizers

Burning of coal, Fuel combustion Smoking

Chemical manufacturing, burning of rubber tyres, sludge, sewage

Fig. 12.1 Various sources of polycyclic aromatic hydrocarbons

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white-rot fungus, and its substrate are used to recycle Nigerian oil drill cuttings containing PAH under laboratory conditions (Okparanma et al. 2011). Healthy soil shelters plants and microorganisms. Treatment of soil is making it unsuitable for plant nourishment. Both ligninolytic and non-ligninolytic fungi can break down PAHs by extracellular lignin-degrading enzymes. Species belonging to Aspergillus, Penicillium, Rhizobium, and Trichoderma can degrade PAHs (Aydin et al. 2017). Toxic soil was collected from a diesel eroded site; naphthalene (a PAH) was chosen for hydrocarbon degradation studies. DNA barcode identified the involvement of Fusarium oxysporum in it (Romauld et al. 2019). Bhatt et al. (2002) selected two white-rot fungi I. lacteus and P. ostreatus for inspecting the degradation of polycyclic aromatic hydrocarbons in contaminated industrial soils. Ecotoxicity assay had also been executed and it was observed that they degraded fluorene, anthracene, chrysene, and pyrene in contaminated places. P. chrysosporium was able to degrade fluorene in the soil (George and Neufield 1989). Vyas et al. (1994) said that anthracene was degraded up to 60% by white-rot fungi. They oxidized anthracene (AC) to anthraquinone (AQ). AQ was also found to degrade further in some selected cultures of white-rot fungi. Fungi implement monooxygenase enzyme-mediated polycyclic aromatic hydrocarbon degradation (Gupta and Pathak 2020). Mahajan et al. (2021) showed that PAH is xenobiotic. Studies were conducted in the Gulf of Kutch and the surrounding coastal areas of Gujarat. Fungal growth was observed in the collected samples. The isolates of P. ilerdanum and Aspergillus showed around 75% ability to degrade several PAHs. Pycnoporus sanguineus degraded roughly 70% of anthracene. Extracellular laccase and cytochrome P450 enzyme played role in this (Zhang et al. 2015). P. eryngii was studied for its efficiency in getting rid of manganese and phenanthrene. They removed them by more than 90% in a half-a-month span (Wu et al. 2016). Synthetic surfactant, tween 80, enhanced the mycoremediation process as compared to plant-based surfactant saponin. Marine fungi and Marasmiellus species displayed an increased level of pyrene and BaP degradation. It degraded pyrene completely without generating toxic compounds (Vieira et al. 2018). PAHs are present in the marine environment, but their degradation plans are not quite understood. Fungus improvised cytochrome P450 and epoxide hydrolases for toxin degradation. PAHs have low solubility in water and it can be enhanced by using surfactants to reduce the surface tension (Lamichhane et al. 2017). Surfactants have hydrophobic and hydrophilic moieties. They fill the gap in the little information about surfactant enhanced remediation (SER) of PAHs. Tween 80 has already been preemptively widespread as a surfactant. In T. versicolor, PAH degradation was raised by tween 80 and it degraded fluorene, anthracene, phenanthrene, and pyrene (Rodríguez-Escales et al. 2013). SER is a noteworthy technique to treat the PAH in the soil and aquatic environment with the support of surfactants that are either synthetic or natural (biosurfactant). Agrawal et al. (2018) used Ganoderma lucidum for the biodegradation of phenanthrene and pyrene. They were able to degrade at least 90% of these with ligninolytic enzymes. The mechanism of PAH metabolism by non-ligninolytic fungi has been already studied in detail (Gupte et al. 2016). It involves the oxidation of aromatic rings by cytochrome P450

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monooxygenase. Atmosphere receives a higher quantity of PAH by environmental lead (Pb) since lead is now ubiquitous. PAHs expand by the combustion of organic matter. They are cohesive to soil particles and get settled down by landfills and dumping activities of man. Exposure to them leads to asthma, respiratory diseases, deterioration of air quality, and chronic sickness when consumed via food.

12.5

Mycoremediation of Heavy Metals

Heavy metals are naturally occurring elements found throughout the earth’s crust. Their high toxicity levels are due to several factors—their dose and path of exposure. Examples include lead (Pb), zinc (Zn), cadmium (Cd), chromium (Cr), mercury (Hg), and arsenic (As) (Tchounwou et al. 2012). Pleurotus species are universally adopted and high-yielding varieties employed in the mycoremediation process. They have biosorption capacity because of their vast hyphal biomass. Such fungi gather high levels of heavy metals. Biosorption is a process by which heavy metals get absorbed on the surface of the biosorbent (Velásquez and Dussan 2009). Procedures as chelation (extracellular) and binding to proteins (intracellular) lead to heavy metal remediation and endurance in fungi (Fawzy et al. 2017). These methods are for decontaminating polluted environments. Mushroom laccase and manganese peroxidase (MnP) enzymes degrade the lignocellulosic remnants and allow them to grow on agricultural wastes. Accumulation of heavy metal within the fruit body inclines to increase with a rise of the metal in the substrate (Ogbo and Okhuoya 2011). The residue after mushroom harvest is employed for mycoremediation in required contaminated sites. Akhta and Mannan (2020) reported that soil erosion and weathering of the earth’s crust are some natural methods of heavy metal pollution. Anthropogenic activities result in industrial effluents, fertilizers, and pesticides that release tons of heavy metals. They enter the human body via the consumption of contaminated food and water. The accumulation of heavy metals in plants hinders their activities. The effects of some heavy metals on plants are as follow: 1. 2. 3. 4.

Obstruction in the electron transport system (ETS) Decrease in water potential Inhibition of antioxidative defense systems Loss of essential metal ions and inhibition of plant growth

Ion exchange and electrochemical analysis methods are frequently done to dispose heavy metals, but they have their restrictions. Various fungi associated with the genus Aspergillus and Fusarium were isolated from land contaminated with arsenic. They could tolerate high concentrations of arsenic (As). Moreover, T. reesei and Fomitopsis meliae can handle copper, cadmium, arsenic, lead, and iron (Oladipo et al. 2018). They can also boost the soil quality. It is crucial to develop methods by which the remediating fungi are pulled out as they accumulate metal ions inside them. Heavy metal pollution renders negative consequences on soil and crop quality. Galerina vittiformis was functional in eradicating Cu, Pb, Cd, and Zn

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within a month in a district of Karnataka, India (Damodaran et al. 2013). Marasmius oreades can remove bismuth and titanium (Elekes and Busuioc 2010). Microorganisms have unfolded several mechanisms to change or reduce the toxicity of metallic contaminants through pH change, biosorption, or bioaccumulation. In bioaccumulation, enzymes are actively transported within and outside the cell and create vacuoles where metal ions are gathered and immobilized. Production of metal-binding compounds takes place. Khan et al. (2019) isolated specific fungal strains of Aspergillus from lead and mercury-contaminated industrial sites. Aspergillus (M and M7) strains could be used for in situ or ex situ remediation of lead and mercury-contaminated soil. de Wet et al. (2020) reported that A. piperis is an applicable candidate for bioremediation of lead, copper, manganese, and magnesium. He proved it through the agar well diffusion method. Pihurov et al. (2019) stated some challenges faced in incorporating fungi as bioremediators: 1. Difficulty in producing fungal inoculum in bulk amounts. 2. There should be accuracy in the application of inoculum for obtaining ample growth in soil. 3. Choice of a carrier material. 4. Piling up heavy metals in soil declines the produce. Numerous fungi are microscopic in the soil and play a relevant role in recycling complex organic compounds and might tolerate heavy metal metalloids (Chan et al. 2016). A peculiar cell wall structure furnishes fungi with metal binding property (Gupta et al. 2000). Cell surface sorption of metals and metalloids is a repercussion of physicochemical interaction between the metal ions and the functional groups on cell surface proteins (Dhankhar and Hooda 2011). Heavy metals are exclusively collected within fungal cell walls in the form of precipitates such as oxalates, phosphates, and sulfates (Wei et al. 2013). Channeling of heavy metals to fungal cell walls can be assisted by siderophores. They enhance the mobility of heavy metals such as Cd, Cu, Zn, and Pb (Schalk et al. 2011). Antioxidant enzymes also play an extensive role in responses to metal vulnerability (Raab et al. 2004). These enzymes have been claimed to displace reactive oxygen species from fungi. They restore the impairment caused by reactive oxygen species (Bai et al. 2003). The synergy of biosynthesis of nanomaterials and the possibility of fungi to oust toxic metals from contaminated land have been suggested by many researchers. Fusarium species isolated from a Zn-contaminated mine in South Korea were able to absorb up to 320 mg/L of zinc and have the ability to produce zinc oxide nanoparticles (Velmurugan et al. 2010). P. eryngii can remove aluminum oxide nanoparticles up to around 90% (Jakubiak et al. 2014). Kumari et al. (2019) stated that Cladosporium species have very high absorption power and can easily absorb heavy metals such as lead, nickel, chromium, and arsenic. Komagataella phaffii mitigates contamination of cadmium, chromium, and lead (Liaquat et al. 2020). It had raised tolerance against increasing levels of these heavy metals. Biosorption is the binding and concentration of heavy metal from an aqueous solution by microbial biomass. Adsorption is subject to pH and dose (Prasad et al. 2013). Approximately 90% of lead (Pb2+)

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was withdrawn by T. viride at a pH of 6 and 100% at pH 7 by P. florida. It is pertinent to get rid of lead from wastewater. Ligninolytic enzymes actively participating in their degradation were expressed in the presence of the substrate. A variety of investigations were performed using P. chrysosporium, which degrades a high number of organic pollutants (Pointing 2001). The existence of heavy metals in soil is catastrophic for agronomic businesses and consumers. The use of pharmaceutical compounds (PhC) has increased over time. They are resistive to degradation by light, water, and chemical compounds that produce them. They are hard to handle when liberated within the aquatic ecosystem. Solid-state fermentation, a biological procedure based on living microbes, has stimulated curiosity due to its minimal environmental damage. It presents several gains because it takes place under requirements for the expansion of filamentous fungi like white-rot fungi (Thomas et al. 2013).

12.6

Mycoremediation of Plastics

Polythene is the chiefly used plastic across the globe. Among the complete plastic waste produced, polythene contributes the maximum share of 65%. Synthetic plastic is nonbiodegradable. Polythene or polyethylene is a polymer of ethylene gas. Terrestrial animals unknowingly consume discarded plastic bags together with commercial waste, which is fatal for them. Polythene shows detrimental consequences on all the major kinds of biomes. A different plan of action is needed to cope with the ever-increasing rate of plastic waste. Use of bioremediation is an eco-friendly and long-lasting method for their degradation. Most effective polythene deteriorating fungal isolates are known to be of Aspergillus strains. Sangale et al. (2019) collected some samples to isolate polythene degrading fungi from coastal regions of India. It has been reported that the breakdown of polythenes was a crucial part of the degradation path followed by ligninolytic fungi. Primary degradation terminates in the genesis of methane, carbon dioxide gas, and water (Grover et al. 2015). Commercial fields have relied on plastic production, but major difficulties lie in modern times because of their imperishable nature, which is tricky to manage. Marine biology is adversely affected by plastic dumps. It is often problematic for all folks as microplastics are ingested by marine organisms, getting somewhere incorporated into the food chain phenomenon. Munir et al. (2017) made frequent attempts to downplay the aggregation of plastic waste within the environment over some decades. Microbial degradation of plastics has been holding much notice lately because of the pressure on developing countries to curtail plastic waste. Filamentous fungi like Trichoderma and Aspergillus have promising leads to the longer term of plastic degradation strategies. Mushrooms like P. tuber-regium grow swiftly on media having polythene powder by utilizing it as a carbon and energy source. FTIR analysis shows absorbance at regions near carbonyl groups suggesting that polythene was degraded oxidatively. Monocultures of P. tuber-regium and P. pulmonaris were used within the testing procedure. It may be due to their

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capability of higher production of extracellular enzymes that helped in utilizing the polyethylene powder (Nwogu et al. 2012). Plastic disposal in a landfill may be a method applied to eliminate solid plastic waste. Steady piling up of such wastes in landfills is a concern as plastics take around thousands of years to decompose and therefore the land becomes inferior for residential projects. It also impedes water flow. White-rot fungi, P. ostreatus, could be a strong degrader of lignin and cellulose. Mycelial formulations are noted in the substrate with biodegradation. This was done by combining abiotic and biotic factors and exposing the plastic bags for 4 months in the sun and the other 4 months in fungal incubation (Luz et al. 2020). Raaman et al. (2012) have also reported the usefulness of Aspergillus species and the potential of their various strains in polythene degradation. Plastics have greater tensile force. Indiscriminate use of plastic bags by people has presented an alarming situation. It is the foremost report on the degradation of rarity polythene (LDPE) under laboratory conditions by A. japonicus. Polyurethanes aid in environmental issues because of belonging to a very repellent polymer family. Their degradation may be a matter of question for sustainable waste management strategies. They need a negative impact on terrestrial and water bodies. Fungi are more effective in their degradation as compared to bacteria. Magnin et al. (2018) isolated 30 strains of fungi from polyurethane wastes. Some species of Alternaria and Penicillium utilized polyurethanes as a carbon source and these species were found to be helpful. Polyurethane treatment may be a challenge within the current scenario. Penicillium species proved to be more important in handling plastic pollution. An enormous number of health care institutes and hospitals are producing enormous biomedical waste. Biomedical waste generation by hospitals may be a huge problem as its management requires power expenditure and warm temperature treatments. Most health care centers install incinerators for quick treatment and management of biomedical waste generated in their respective hospitals. Incineration methods unleash smoke and ash into the environment resulting in system and cancer issues. These procedures are extravagant, liberating toxic compounds such as dioxins, furans, and ash. Coprophilic fungi, Periconiella species (found in cow dung), were employed for the degradation of medical wastes. It is a cheap and less demanding method for biomedical and plastic waste degradation. The biomedical scrap was smeared on the pure culture of the fungal species. The degradation started on the fourth day. It can degrade plastic from the ninth day without polluting the environment (Deshkar et al. 2019).

12.7

Mycoremediation of Dyes and Agricultural Contaminants

P. chrysosporium was the primarily described fungus to be ready to degrade synthetic dyes (Ruiz et al. 2018). Turquoise blue dye was learned as a pollutant and the efficiency of P. ostreatus was evaluated for its degradation. Detoxification of malachite green and fuchsin was observed by A. niger and P. chrysosporium (Rani et al. 2014). Different chemical methods are used for the remediation of colored effluents, especially in textile industries. The key advantage of those fungi in dye

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degradation relies on the oxygenation of the fungus and gradual contact of released enzymes with the molecules. Biodegradation occurs due to disruption of the chromophore in dye molecules because of extracellular enzyme formation by fungi. Rodríguez et al. (1999) purified laccase enzyme from T. hispida and watched its decolorization act. Lignin and manganese peroxide enzymes were found to play the part. Distinct industrial dyes were decolorized biocatalytically by extracellular enzymes from different strains of white-rot fungi (Table 12.1). Textile dye effluents discarded into the aquatic habitats increase the biological oxygen demand. The requirement of an enormous amount of water in cloth manufacturing units is deleterious as the wastewater gets enriched chemically. Poor handling of dyes ends up in contaminated habitats as plenty of harmful metals are present in them (Singh 2017). Kuhar et al. (2015) illustrated malachite green combined and solo degradation by G. lucidum and T. versicolor. Jimenez et al. (2018) estimated the performance of fungal segments in dye degradation. P. pulmonaris, P. ostreatus, T. versicolor, and plenty of other white-rot fungi were tested. Usage of fungal consortia has not caused a synergy between the species to amend the bioremediation of dyes. It can be discovered through the race for space or nutrients between selected species in solid-state fermentation (SSF) that microorganisms need a definite area to grow that starts to be restricted when one species uses the identical substrate for growth. T. reesei isolates metabolized benzo alpha pyrene with glucose as a co-metabolite substrate in a PAH-contaminated soil (Yao et al. 2015). Nonidentical strains of Aspergillus and Fusarium were isolated Table 12.1 Decolorization of a few dyes using White-Rot Fungi WRF Cladosporium cladosporoides

Dye Synthetic dyes Azo dyes and triphenylmethane dyes

Phanerochaete chrysosporium

Azo dyes [Red-80 and Mordant Blue-9]

Coriolus versicolor

Textile effluents

Pleurotus ostreatus

Remazol Brilliant Blue Royal

Pleurotus ostreatus

Acid Orange 7, Acid Orange 8, Mordant violet 5 Direct Red 80

Pleurotus ostreatus Pleurotus ostreatus and Stereum ostrea Cordyceps militaris Pleurotus pulmonaris

Triphenylmethane Dye Reactive Green 19, Reactive Yellow 18, Reactive Red 31, Reactive Red 74 Malachite Green, Brilliant Blue, Phenol Red Coomassie, Victoria Blue B

References Nilsson et al. (2006) Vijaykumar et al. (2006) Singh and Pakshirajan (2010) Asgher et al. (2009) Erkurt et al. (2007) Lu et al. (2008) Singh et al. (2009) Usha et al. (2020) Kaur et al. (2015) Sanga et al. (2018)

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from soil contaminated with arsenic and reduced arsenic under in situ conditions (Singh et al. 2015). The chemical and physical properties of soil such as pH, temperature, and water availability add adequately to the microbial domain in the soil besides the success of the bioremediation process. Filamentous fungi can cause the degradation of pharmaceutical compounds at a relatively faster rate than bacteria (Agunbiade and Moodle 2014). Accessibility to the contaminants hastens the process. Many fungi generate biosurfactants that assist in the alteration of contaminants (Prakash 2017). Additionally, litter-degrading fungi too help out in breaking down soil organic matter. Lindane is an imperishable chlorinated insecticide. It has been employed in the agriculture field for pest control prior to being banned. It lasts long within the environment and gathers in fat tissues due to the greater dissolving power in lipids (Zucchini-Pascal et al. 2009). The efficiency of white-rot fungi to degrade the insecticide lindane (a chlorinated insecticide) was observed in T. versicolor and Pleurotus species (Ulčnik et al. 2012).

12.8

Advances in Mycoremediation Technology

Evolutionary biology techniques like transcriptomics, proteomics, and metagenomics have ushered in better environmental management plans (Plewniak et al. 2018). Multi-omics studies conducted as a single omics program cannot reveal all the functional and physiological activities of any community (Meena et al. 2018). Metagenomics analysis begins with the nucleic acid separation of the collected samples. Transcriptomics enlightens us about the regulation of gene mRNA expression. Microarray and sequencing techniques are engaged in this tool. Microarray throws light on gene expression. DNA microarray is a widely used technique in transcriptomics. It gives an insight into every gene that constitutes a living being and its mRNA expression (Maroli et al. 2018). Proteomics is the set of proteins found inside an organism that is known as the proteome. It includes posttranslational modifications and metabolism paths inside the cell. It has made possible the discovery of proteins present in microorganisms at contaminated sites. Community-level proteome examination is known as metaproteomics. Community proteome extraction involves the following: • Cell fractionation • Protein extraction via ultrasonication • Generation of protein pool • Protein identification

Protein obtained is identified by gel electrophoresis methods or by enzymatic digestion followed by mass spectra analysis using modern technical analysis such as LC-MS/MS. The ultimate steps are protein identification and data interpretation (Chandran et al. 2020). Metabolomics is the study of metabolites account of a cell

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High throughput data

Bioinformatic studies

In silico processing Contaminated land/water body

Isolation of microorganisms from the site

Genomics

ƒ ƒ ƒ

Upgraded Mycoremediation strategies

Transcriptomics

Epigenetic ƒ modifications Gene sequencing Regulatory motifs ƒ ƒ

Posttranscriptional modifications m-RNA expression Protein-DNA interaction

Proteomics

ƒ ƒ ƒ

Post-transitional modifications Protein expression Protein structure

Metabolomics

ƒ

Metabolic pathways

Fig. 12.2 Illustrating modern omics approaches

(Fig. 12.2). Under stress conditions, cells of living beings secrete various metabolites to cope up. The metabolomics approach analyses the effect of environmental conditions on metabolites (Malla et al. 2018). It may help understand the primary and secondary metabolites emitted by microorganisms when subjected to contaminated areas and check their stress response. The discovery of a conserved and varying gene sequence, 16S rRNA, has reformed molecular biology. Phylogenic and analogical experiments are conducted to differentiate closely related microorganisms. Further, it is being incorporated to study the microbial diversity isolated from contaminated sites (Lovely 2003). Two mainstream advances in remediation technology are biostimulation and bioaugmentation methods. Bioaugmentation is the inclusion of favorable microbes. The fungal cell wall is rich in chitin, a polymer of N-acetyl Dglucosamine that intensifies metal intake. Supplemented microorganisms can metabolize a particular pollutant when added to the soil. In fungal augmentation, superior inocula are developed. In biostimulation, nutrients, electron acceptors, or donors are injected into the contaminated areas to arouse the degrading property of microbes.

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The shortcoming of biostimulation is that if the toxicity levels within the soil are high, the indigenous microbes might not be sufficient. In bioaugmentation, there is a possibility that the induced microbial population might not be able to survive in the new environment.

12.9

Conclusion and Prospects

Integrated practice is a combination of two different methods to achieve a collaborative and constructive plan to treat noxious compounds. The positive link among the environmental components serves as the basis for all living organisms but leaps in science and technology have contributed to the pollution of resources. Lesser knowledge on proper disposal of effluents and negligence to implement strict regulatory standards by policymakers have added to the worsening of resources. The physiochemical treatment methods exercised to rectify contaminated sites are flawed when it comes to larger-scale implementation. It will be solved by integrated processes that are of a fixed duration, nonpolluting, and achievable. The endemic fungi growing in polluted habitats should be investigated for futuristic studies as they are accustomed to the higher concentration of pollutants, which will help in more organic technology buildup. It is not very easy to completely get rid of contamination but synergistic approaches have such potential. The application of ligninolytic fungi and their enzymes could be beneficial. Recombinant DNA technology can be applied to upgrade the genetic material of fungi for their use in mycoremediation. Establishment of Genetic microbial tools to decay pollutants needs to be analyzed. Genetically modified cultures have a rich effect on the ecosystem. Some pollutants are mild but catastrophic. The biosorption mechanism also requires future research. Additional studies should be done to address the gap in the methods employed by fungal communities in the bioremediation process. Interdisciplinary methods are needed to focus on either the regeneration of biomass or the retrieved metal being converted to a fruitful form. Omics approach carries the prospective to assume the metabolism of fungi in polluted areas. They bring a new vision to record mechanisms included in polycyclic aromatic hydrocarbons, heavy metal, and chlorinated compounds remediation at the species or community level. Bioinformatic tools together with metabolomics have empowered a thorough perception of mechanisms operating inside microbial communities and the genes accountable. Metabolite detection is done by combining bioinformatics software and analytical methods. Progress in nanotechnology might help in studying the role of membrane-associated oxidoreductases in alleviation by white-rot fungi. The fungal biomass eliminated from fermentation processes is used in the mycoremediation process. Regardless of being new, there are a lot of possibilities for research in this field. We are capable enough to discover new dimensions. We only need a proper endorsement, management skills, implementation strategies, and sharp resources!

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Exploration of Plant Growth-Promoting Rhizobacteria (PGPR) for Improving Productivity and Soil Fertility Under Sustainable Agricultural Practices

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Gowardhan Kumar Chouhan, Saurabh Singh, Arpan Mukherjee, Anand Kumar Gaurav, Ayush Lepcha, Sudeepa Kumari, and Jay Prakash Verma Abstract

Under green revolution practices, the imbalanced use of chemical fertilizers and pesticides causes a negative impact on soil health due to the loss of soil microbial flora and fauna. To overcome this negative impact of the green revolution and to increase sustainable agricultural production without damaging further agricultural lands, the only alternative and effective means is to reduce the use of chemicals in agriculture specifically for plant nutrition and plant protection. Under sustainable agricultural practices, plant growth-promoting rhizobacteria (PGPR) can be effective tools to increase productivity while ensuring sustainability in agriculture. PGPR colonize the rhizosphere zone and help in promoting plant growth and development by regulating nutrient acquisition, modulation of plant hormones, and ameliorating various negative effects of various pathogens. PGPR also help sustain the plant growth productivity and significantly increase soil fertility and health under different biotic and abiotic stresses. As per the literature, many studies prove to increase agriculture productivity due to the use of PGPR as eco-friendly microbial inoculants for promoting plant growth attaributes through various direct and indirect mechanisms. The mechanisms of PGPR include biological nitrogen fixation, phytohormones production, Phosphate, potassium, and zinc solubilization, siderophores production, and secretion of other secondary metabolites (phenolic compounds (phenylpropanoids and flavonoids)) that enhance crop productivity and control phytopathogens. Therefore, this chapter focuses on a detailed description of PGPR keeping in view their functional mechanisms as eco-friendly approaches to increase productivity and enhance

G. K. Chouhan · S. Singh · A. Mukherjee · A. K. Gaurav · A. Lepcha · S. Kumari · J. P. Verma (*) Institute of Environment and Sustainable Development, Banaras Hindu University, Varanasi, Uttar Pradesh, India e-mail: [email protected] # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2022 U. B. Singh et al. (eds.), Re-visiting the Rhizosphere Eco-system for Agricultural Sustainability, Rhizosphere Biology, https://doi.org/10.1007/978-981-19-4101-6_13

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soil fertility. PGPR can be used as an eco-friendly, socially acceptable, and costeffective technology for challenges in the future.

13.1

Introduction

Microorganisms inhabiting almost every part of the biosphere support the life system on the planet Earth. At present, there is limited knowledge about the microbial world of the Earth’s crust and its members that are present in the environments such as soil, water, and air. These microorganisms can live either in an individual plant or in specific plant organs (e.g., roots, shoots, leaves, seeds, nodules, sprouts of legumes, flowers, and fruits). Other than that, the microorganisms reside in a narrow zone of soil, influenced by plant roots, and are associated with roots and the rhizosphere (Rout and Southworth 2013; Chouhan et al. 2021c; Mukherjee et al. 2019, 2020a, b). The plant-associated microbes migrate from bulk soil to the rhizosphere region of plants (Kloepper 1978). These rhizosphere bacteria act as symbionts for plants and considered plant growth-promoting rhizobacteria (PGPR) (Kapulnik 1991). Plants secrete flavonoids such as amino acids and sugars that provide a rich source of energy and nutrients for the microorganisms, which results in higher bacterial population in the rhizosphere region as compared to the non-rhizosphere region. A variety of bacterial genera are present in this region, most commonly species of Pseudomonas, Arthrobacter, Bacillus, Erwinia, Flavobacterium, Burkholderia, Caulobacter, Serratia, Hyphomicrobium, Micrococcus, Agrobacterium, and freeliving nitrogen-fixing bacteria (Azotobacter and Azospirillum) (Foster et al. 1983; Prithiviraj et al. 2003; Gray and Smith 2005; Mukherjee et al. 2020a, b). Rhizobacteria represent an important group of microorganisms and show more intimate associations with plant roots referred to as endophytes (Hardoim et al. 2015). Most members of bacterial taxa have been isolated from the endorhizospheric region, comprising endophytic species (Hallmann and Berg 2006). The bacterial taxa present within this region include species of Pseudomonas, Enterobacter, Bacillus, Burkholderia, and Azospirillum. There are a number of factors involved in the establishment of the rhizosphere and endophytic microbiome (Lakshmanan et al. 2014). It depends upon soil and host type (Bulgarelli et al. 2012; Lundberg et al. 2012). There are, however, other factors such as biotic and abiotic circumstances, climatic conditions, and anthropogenic effects that also play important roles in microbial population dynamics in specific plant species and soil types (Lakshmanan et al. 2014).

13.2

Rhizosphere

The term rhizosphere was first coined by Lorenz Hiltner (Hiltner 1904). The rhizosphere is the narrow area around the root surface that supports highly diversified microbial activity (Fageria and Stone 2006; Lakshmanan et al. 2014).

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Based on the microbial colonization, the rhizosphere area can be categorized into three zones, namely, rhizosphere, rhizoplane, and endorhizosphere. The rhizosphere microbiomes are influenced by the quantity and quality of root exudates. The rhizoplane is the root surface strongly associated with soil particles. The endorhizosphere is the interior part of the root that is inhabited by some specific type of microbes called endophytes (Barea et al. 2005). Highly diversified microorganisms that compete with each other to occupy space and food (Raaijmakers et al. 2002) colonize the rhizosphere zone. Therefore, these microorganisms could be beneficial or pathogenic to the associated plant. Mutualistic symbionts of the rhizosphere microbiome colonize the plant tissue and obtain nutrition and in return they provide factors for the enhancement of growth and development of the host plant (Haas and Keel 2003). Different kinds of interactions take place in the rhizosphere that can occur between plant–plant, microbe–microbe, plant–microbe, and interaction with other eukaryotic microbes (De-la-Peña et al. 2012). To reveal the complex interactions between these microorganisms, there is a need for the development of an understanding of the chemical communication between plants and their rhizosphere microbes as to how they coordinate their behavior and interact with each other. A number of studies have been carried out on molecules and the mechanisms of microorganisms that addressed their coordination in the rhizosphere with the plant growth and productivity (Pieterse et al. 2009; Miller and Oldroyd 2012; Morel and Castro-Sowinski 2013; Rosier et al. 2018). Microorganisms associated with rhizosphere function as plant growth-promoting rhizobacteria (El-Tarabily et al. 2008; Merzaeva and Shirokikh 2010), as anti-phytopathogenic through their activities such as protecting the plant from disease (Kloepper et al. 2004) and making nutrients available to the plant (Pradhan and Sukla 2005; Martínez-Hidalgo et al. 2014). Despite many reports on rhizosphere microbes, communication mechanisms and interactions between different taxa and different communities are largely unknown.

13.3

Plant Growth-Promoting Rhizobacteria (PGPR)

Plant growth-promoting rhizobacteria are the microbes that aid plants in their growth through direct and indirect mechanisms such as nitrogen fixation, production of phytohormones, and various other secondary metabolites as attributes of biocontrol agents (Mukherjee et al. 2020a, b, 2021a, b, c). Rhizobacteria affect plant growth and metabolism in multiple ways, such as regulating the nutrient acquisition, modulation of phytohormones, and ameliorating negative effects of various pathogens and also different abiotic stresses (Fahad et al. 2015; Chouhan et al. 2021a). PGPR have also been shown to help in the remediation of the environment through detoxification of various heavy metals, such as arsenic and cadmium, and also pesticides, such as monocrotophos and chlorpyrifos. The process of enhancement of plant growth and development by the PGPR is achieved through the modulation of plant and soil chemistry, which is aided by the regulation of various hormones and nutrients (Nadeem et al. 2014). PGPRs are also known to ameliorate

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the negative effects of various abiotic stresses such as salinity stress and heavy metal stress through the production of different secondary metabolites.

13.3.1 Functional Attributes of PGPR for Sustainable Agriculture The functional properties of PGPR are of two types, that is, direct and indirect mechanisms. The direct mechanism includes biological nitrogen fixation, solubilization of phosphate, zinc, potassium, and other minerals, and production of phytohormones, ammonia, and siderophore (Fig. 13.1) (Mukherjee et al. 2020a, b). The indirect mechanisms are the production of hydrogen cyanide (HCN), chitinase, antibiotics, and various other secondary metabolites produced for biocontrol of disease-causing agents (Mukherjee et al. 2020a, b). These functional properties are very useful for enhancing plant growth attributes and soil fertility, and health contributing to sustainable agricultural production. The production of various secondary metabolites helps in the amelioration of the different abiotic stresses such as salinity stress and drought stress (Sunita et al. 2020; Chouhan et al. 2021b). The nitrogen-fixing rhizobacteria present around the roots of the leguminous plants cause the formation of root nodules to help in fixing atmospheric nitrogen and making nitrates available to the plants. The production of ammonia is an important aspect of PGPR to support nitrogen nutrition and thereby increase crop productivity. The production of HCN by microbes protects plants from soilborne phytopathogens (Hayat et al. 2010). The PGPRs also enhance nutrient acquisition

Fig. 13.1 Mechanisms of plant growth-promoting rhizobacteria for sustainable agriculture

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and can be used as nutrient solubilizers. Microbial species such as Azotobacter, Pseudomonas, Bacillus, Burkholderia, Enterobacter, and Azospirillum are wellreported PGPR strains known to promote plant growth effectively through increased uptake of nutrients (Mukherjee et al. 2020a, b, 2021a, b, c; Rasool et al. 2021). Other functional attributes of the PGPRs can be the minimization of the deleterious effects posed by pathogens and stress conditions and enhancing plant growth simultaneously (Safdarian et al. 2020).

13.3.1.1 Biofertilizer Indiscriminate use of chemical fertilizers and pesticides in agricultural production has disturbed various ecosystems. Synthetic chemicals contaminate the environment, increase soil salinity, and also decrease the nutritional quality of food products. The increased chemical contents in soil indirectly lead to an increase in greenhouse gas emissions, thereby increasing climate change concerns. They make it more vulnerable to plant pathogens by weakening the root system. The symbiotic association of the plants and microbes plays a significant role in the biofertilizer industry. It can help boost agricultural production with its management in a sustainable way. Nitrogen from the atmosphere is converted to ammonium and nitrate and made available to the plants. Microbes such as Rhizobium, Azorhizobium, and Sinorhizobium act as biofertilizers (Prasad et al. 2019). Recently, a large number of biofertilizers have been used to harness the symbiotic relationship between microbes and their host plants in boosting crop production under sustainable agriculture (Kumar et al. 2009). However, detailed studies are required under adverse biotic and abiotic conditions such as drought, salinity, high soil temperatures, adverse soil pH, and presence of organic acids to understand the mechanism and also enhance fertility and crop production through biofertilization process. Biofertilizer is a microbial culture developed in solid and liquid bioformulation for boosting crop productivity. This can be used for multiple plant growth-promoting agents that directly and indirectly enhance plant growth attributes and productivity. Liquid biofertilizer is more effective than solid biofertilizers due to more cell viability and effectiveness. Biofertilizers are used as seed, soil, and root dip treatments for enhancing agricultural productivity in a truly sustainable way.

13.4

Mechanisms of PGPR

13.4.1 Biological Nitrogen Fixation (BNF) Nitrogen is a crucial element present in many compounds of the plant playing a vital role in plant growth, which can be fixed by both Rhizobium and some free-living bacteria in soils and plants. Nitrogen fixation is a process through which microbes can fix atmospheric N2 and provide it to plants for their use. The nitrogen fixation process is catalyzed by specific symbiotic, nonsymbiotic, or endophytic microbes. More than 80% of nitrogen is present in the atmosphere but is unavailable to plants. Only some microbes are able to convert gaseous nitrogen to ammonia and nitrates

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and make it available to the host plant (Franche et al. 2009). A diazotrophic enzyme, nitrogenase causes the conversion of atmospheric nitrogen to ammonia. These microbes show complex interactions with leguminous and nonleguminous plants to form a nodule. Among diazotrophs, rhizobia-legume symbiosis is the most studied in agriculture systems (Fenchel et al. 2012). In addition to symbiotic bacteria, many bacteria present in the rhizosphere have the ability to fix atmospheric (e.g., Bacillus, Acetobacter, Alcaligenes, Arthrobacter, Azospirillum, Azotobacter, Corynebacterium, Beijerinckia, Clostridium, Derxia, Enterobacter, Klebsiella, Rhodospirillum, Xanthobacter, Pseudomonas, and Rhodopseudomonas) (Latt et al. 2018) (Table 13.1).

13.4.2 Phosphate Solubilization Phosphorus is the second most important element for plant growth, which is required by the plant in higher quantities. Phosphorus is necessary for various processes including DNA and RNA synthesis. Most of the phosphorus is found in an insoluble state in the soil, being not readily available to plants. Plants obtain phosphorus in the soluble form such as HPO4 2 and H2PO4 1, which depends on the pH of the soil (Rodrıguez and Fraga 1999; Richardson 2001). To fulfill the deficiency of phosphorus, chemical fertilizers are used in soil but a great amount of phosphorus is again converted into less available forms by the process of precipitation with other elements such as Al, Fe, and Ca. The precipitation of phosphorus depends on the pH of the soil (Stevenson and Cole 1999; Richardson 2001). Approximate 40% of phosphorus can be solubilized by bacterial culture (Richardson 2001). Many microbes can solubilize the phosphorus in a simpler form and make it available to the plant and hence are called phosphate solubilizing microbes (Rodrıguez and Fraga 1999). A diverse number of microbes have been reported that solubilize phosphorus. They include species of Pseudomonas, Bacillus, Rhizobium, Burkholderia, Achromobacter, Agrobacterium, Micrococcus, Aereobacter, Flavobacterium, and Erwinia (Bardiya et al. 1974; Chen et al. 2006; De Freitas, et al. 1997; Dey 1988; Richardson 2001; Rodríguez and Fraga 1999; Verma et al. 2010, 2017; Mukherjee et al. 2020a, b). Phosphorus is a limiting factor for plant growth mainly for legume plants (Raman and Selvaraj 2006). However, the mechanism of phosphorus uptake by PGPM and induced plant growth is not known (Mukerji et al. 2006). PSB may decrease the pH of the soil by producing many organic acids such as citrate, lactate, and succinate. Some species of rhizobacteria have been investigated for their ability to convert glucose to gluconic acid by their membrane-bound enzymes and ultimately into 2-keto-gluconic acid (Mukerji et al. 2006; Verma et al. 2017). However, the organic acid secreted by plants presumably has the capacity to solubilize P than the acid secreted by rhizobacteria (Jones 1998). A variety of organic substrates are reported that can be a major source of P for plant growth. It can be possible when the organic substrate is converted to inorganic P with the help of acid and alkaline phosphatase enzymes. Since soil pH ranges from acidic to neutral value, in this environment acid phosphatases may work efficiently (Rodríguez and Fraga 1999).

T. aestivum

T. aestivum

B. cereus, Serratia marcescens, and P. aeruginosa

Alcaligenesfaecalis

Mucuna pruriens L.

Triticum aestivum L.

Arthrobacter aurescens, B. atrophaeus, Enterobacter asburiae, and Pseudomonas fluorescens Bacterial isolates

Mitigation of salinity stress

Mitigation of salinity stress

Promote growth, regulate Na+/K+ balance, and decrease ethylene emissions in plants Mitigation of drought stress

Biocontrol activity—Sclerotium rolfsii and Fusarium oxysporum

Crocus sativus L.

Brevibacterium frigoritolerans (AIS-3), Alcaligenes faecalis subsp. phenolicus (AIS-8) and B. aryabhattai (AIS-10)

(continued)

Babar et al. (2021)

Desoky et al. (2020)

Safdarian et al. (2020) Brunetti et al. (2021)

Rasool et al. (2021)

Activity PGPR-assisted phytoremediation

Plant tested Solanum nigrum L.

Plant growth-promoting bacteria Bacillus strains

Reference He et al. (2020)

Exploration of Plant Growth-Promoting Rhizobacteria (PGPR) for. . .

Table 13.1 Plant growth-promoting rhizobacteria, its mode of action, and possible outcome Mode of action Inoculation with QX8 and QX13 also enhanced the dry weight of shoots (1.36and 1.7-fold, respectively) and roots (1.42- and 1.96-fold, respectively) of plants growing in cd- and Pb-contaminated soil and significantly increased total Cd (1.28- to 1.81-fold) and Pb (1.08- to 1.55-fold) content in aerial organs compared to non-inoculated controls The PGPR enhanced plant growth through the production of plant hormones and also checked the growth of phytopathogens Upregulation of H+-PPase, HKT1, NHX7, CAT, and APX expression in roots Lower root ACC content ( 45%) in water-stressed inoculated plants, maintain higher levels of both isoprene emission, and carbon assimilation Indole-3-acetic acid (IAA) and hydrogen cyanide (HCN) productions, N2-fixation, and P solubilization enhanced. Maintained ionic imbalance by regulating Na+ and K+ ions and significantly increased growth parameters and plant biomass by

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Plant growth promotion in an intercropping system Plant growth promotion

Cajanus cajan Phaseolus vulgaris L.

Bacopa monnieri (L.)

Oryza sativa

Chickpea (Cicer arietinum L.)

Enterobacter sp. C1D, Pseudomonas sp. G22, Rhizobium sp. IC3109 P. Alcaliphila and P. hunanensis

P. Plecoglossicida, Acinetobacter calcoaceticus, B. flexus, and B. safensis

Flavobacterium sp.

P. putida NBRIRA

Improvement in drought stress tolerance and enhancement in chickpea

Mitigation of salinity stress and plant growth promotion

Mitigation of salinity stress and plant growth promotion

Activity

Plant tested

Plant growth-promoting bacteria

Table 13.1 (continued)

Modulation of membrane integrity, osmolyte accumulation (proline, glycine betaine), and scavenging of ROS. Differential expression of genes involved in ethylene biosynthesis (ACO and ACS), salicylic acid (PR1), jasmonate (MYC2) transcription activation, SOD, CAT, APX, and GST (code for antioxidant enzymes), DREB1A (dehydration responsive

decreasing reactive oxygen species induced lipid peroxidation while increased accumulation of osmolyte, photosynthetic pigments and improved photosystem II efficiency as compared to uninoculated plants Cocultivation resulted in a decrease of the exudation of secondary metabolites Nitrogen fixation, solubilization of inorganic phosphate, and production of phytohormones, ammonia, and acetoin Increase in shoot Na+:K+ ratio, shoot and root biomass (fresh and dry weights), soil enzymes, and soil nutrient parameters showed significant positive correlations with the shoot Na+:K+ ratio Increased plant hormone production and maintenance of Na+:K+ ratio

Mode of action

Menon et al. (2020) Tiwari et al. (2016)

Pankaj et al. (2020)

Vora et al. (2021) AlAli et al. (2021)

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Pea (Pisum sativum)

Corn (Zea mays L.)

Arabidopsis thaliana

Medicago truncatula

Cotton

Rhizobium sp.

Bacillus spp.

B. methylotrophicus M4–96

P. fluorescens strains

P. putida Rs-198

Plant protection and promotion against salt stress

Biocontrol and plant growth promoting activities

Biostimulation of plant growth and development

Plant growth and nutrient enhancement

Plant growth promotion

Facilitates nutrient acquisition such as nitrogen, phosphorus, and iron essential for plant development IAA production, production of bacterial volatile compounds such as four classes of compounds, including 10 ketones, 8 alcohols, 1 aldehyde, and 2 hydrocarbons Production of antifungal volatile compounds such as methanethiol, dimethyl sulfide, DMDS, and dimethyl trisulfide. Plant growth promoting and biocontrol traits such as siderophore production, protease activity, production of indole-3-acetic acid (IAA). Production of phenazines (genephzCD), DAPG (gene-phlD), hydrogen cyanide (gene-hcnAB), and ACC deaminase (gene-acdS) Improvement in production of endogenous indole acetic acid (IAA) content while reduction in abscisic acid (ABA) content under salt stress in cotton

element binding), NAC1 (transcription factors expressed under abiotic stress), LEA, and DHN (dehydrins), which was the result of positive modulation of stress by bacteria IAA, siderophores, HCN, ammonia, EPS

Exploration of Plant Growth-Promoting Rhizobacteria (PGPR) for. . . (continued)

Yao et al. (2010)

Hernández et al. (2015)

Pérez et al. (2017)

Ahemad and Khan (2012a) Calvo et al. (2017)

13 253

Plant tested

Strawberry

S. tuberosum

Greengram

Plant growth-promoting bacteria

B. amyloliquefaciens BChi1 and Paraburkholderia fungorum BRRh-4

B. pumilus str. DH-11 and B. firmus str. 40

Bradyrhizobium sp. MRM6 strain

Table 13.1 (continued)

Abiotic stress tolerance and plant protection

Plant growth promotion and abiotic stress tolerance

Improvement in growth, yield, and content of antioxidants

Activity seedling increase in absorption of the Mg2+, K+, and Ca2+ and decrease uptake of Na+ from the soil Total anthocyanins, phenolics, flavonoids, carotenoids, and antioxidant activities in fresh strawberry fruits were increased It showed enhanced 1-aminocyclopropane-1-carboxylic acid deaminase activity, phosphate solubilization, and siderophore production. Abiotic conditions tiggered enhanced mRNA expression levels of the various ROS-scavenging enzymes and higher proline content in tubers induced by PGPR-treated plants, thus increasing plant abiotic stress tolerance. There was a positive influence of bacterial strain on the PSII phytochemistry of plant, which was confirmed by photosynthetic performance indices Synthesizing of plant growth-promoting substances such as IAA, siderophores, EPS, HCN, and ammonia

Mode of action

Ahemad and Khan (2012b)

Gururani et al. (2013)

Rehman et al. (2018)

Reference

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Bradyrhizobium sp., Pseudomonas sp. and Ochrobactrumcytisi

P. fluorescens

(Cuminum cyminum L.) (Cumin) Lupinus luteus Heavy metal tolerance and plant growth promotion

Biocontrol and plant protection Production of pathogenesis-related enzymes: Chitinase, β1, 3 glucanase, and protease Nitrogen fixation, improvement in plant biomass, and decrease in accumulation of heavy metals in roots and shoots as a bioprotective effect

Rathore et al. (2020) Dary et al. (2010)

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All these reports provide important information about the role of bacterial microbes in making phosphate available to the plant. Therefore, the use of these microbes as a bioinoculant to enhance agricultural production is of great interest to agricultural scientists.

13.4.3 Potassium Solubilization Potassium (K) is available in four forms in the soil and the process of solubilization is mainly done by a wide range of saprophytic bacteria, fungi, and actinomycetes strains (Bakhshandeh et al. 2017). Many studies show that soil bacteria can transform the insoluble potassium into a soluble form that is easily available to the plant (Mukherjee et al. 2019; Meena et al. 2016). There is a considerable amount of potassium solubilizing (KS) aerobic and anaerobic bacteria in soil and mostly KSB are, however, aerobic. The comparatively higher concentration of KSB is present in the rhizospheric region as compared to the non-rhizospheric region (Padma and Sukumar 2015). A number of KSB such as B. mucilaginosus, B. circulanscan, B. edaphicus, Burkholderia, A. ferrooxidans, Arthrobacter sp., E. hormaechei, Paenibacillus mucilaginosus, P. frequentans, Cladosporium, Aminobacter, Sphingomonas, Burkholderia, and P. glucanolyticus have been reported that can solubilize the silicate rocks (Meena et al. 2016). Among KSB in the soil, some potential bacteria such as B. mucilaginosus, B. edaphicus, and B. circulanscan have been reported to possess very effective potassium solubilizing abilities (Meena et al. 2015, 2016). These potassium solubilizing microbes can be isolated from different regions of rhizosphere and non-rhizosphere soil, paddy soil (Bakhshandeh et al. 2017), and saline soil (Bhattacharya et al. 2016).

13.4.4 Siderophore Production (Iron Chelation) Iron (Fe) is the core element for life on earth including plants for their growth and development. Iron acts as a cofactor of many enzymes with redox activity that catalyzes a number of biochemical reactions, which is essential for the growth of nearly all organisms (Sharma et al. 2003; Crowley 2006). For N2 fixation in the leguminous root by the Rhizobium, Fe protein is required for the nitrogenase enzyme (Graham 2005). Siderophore is a low-molecular-weight Fe-chelating compound produced by some microbes in low availability of iron for the plant in soil (Crowley 2006). Many bacteria (Ali and Vidhale 2013) and fungi (Kümmerli et al. 2014; Renshaw et al. 2002) under iron-restricted conditions produce siderophores by producing iron-chelating molecules, and graminaceous plants (Hider and Kong 2010). Diverse microbes are able to synthesize siderophore in the rhizosphere and approximately 500 siderophore structures have been identified (Crowley 2006). Some bacterial genera Bradyrhizobium, Rhizobium, Serratia, and Streptomyces are known to synthesize siderophore in rhizospheric soil. Some plant-associated microbes can also have the capability to form siderophores (Sessitsch et al. 2004).

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The siderophore-producing microbes can be used as a biofertilizer because these make immobilized Fe available to plants and act as a biocontrol agent (Glick 1995). Plants and microbes have evolved a specific mechanism by which they solubilize the insoluble form of Fe with the help of their outer membrane receptor proteins, periplasmic binding proteins, and inner membrane transport proteins in an ironrestricted environment (Matzanke 1991; Sharma and Johri 2003). Previous studies reported that many plant species are capable of using Fe3+ siderophore complexes formed by bacterial microbes (Bar-Ness et al. 1991). Nevertheless, using bacterial siderophores in plant nutrition remains controversial (Vessey 2003). Glick (1995) has shown that the overall requirement of bacterial siderophores by plants is low. The plant cannot use some bacterial siderophores (e.g., pseudobactin and ferrioxamine B) and some siderophore-producing bacteria compete with plants for iron use by producing different types of siderophores (Bar-Ness et al. 1992). Moreover, the siderophore formed by microbes plays a role in biocontrol activities and not just in plant nutrition (Vessey 2003; Mukherjee et al. 2020a, b).

13.4.5 Zinc Solubilization Zinc (Zn) is an important micronutrient required relatively in lower concentrations and is known for its role in catalyzing many metabolic reactions in plants for their healthy growth and development. Zn deficiency in a plant can cause various metabolic problems including a reduction in the formation of carbohydrates, auxins, nucleotides, cytochromes, and chlorophyll, which leads to reduced membrane integrity and ultimately the plant is susceptible to heat stress (Singh et al. 2005; Prasad et al. 2019). Studies reveal that Zn deficiency in crops is not due to the low availability of Zn in soil, but rather it is due to the low solubility of Zn (GontiaMishra et al. 2017). The bioavailability of Zn in the soil is hampered by different factors, such as an increase in the pH, soil organic matter, bicarbonate concentration, high magnesium to calcium ratio, and high availability of phosphorus and iron (Li et al. 2016). Commonly 96–99% of applied inorganic zinc is not used by the plant and is converted into different insoluble forms (Saravanan et al. 2004). These details indicate that the applied Zn fertilizers are readily insoluble and remain in the soil and are not assimilated by the plant leading to Zn deficiency. Zn solubilizing microbes are the potential candidates that can convert the complex forms of Zn to its soluble forms and can thus cater to plant zinc requirements. There are a number of potential microbes that have been reported to increase growth and zinc content when inoculated in crops such as Bacillus sp. (Hussain et al. 2015), Pseudomonas, Rhizobium (Deepak et al. 2013; Naz et al. 2016), and B. aryabhattai strains (Ramesh et al. 2014). Zn solubilizing PGPR help solubilize the complex forms of Zn into soluble forms and make them easily available to the plant leading to the fortification of grains with Zn (Barbagelata and Mallarino 2013). Therefore, Zn is a limiting factor in sustainable agricultural production and Zn solubilizing PGPR are an important candidate for zinc nutrition in plants (Gontia-Mishra et al. 2017).

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13.4.6 Plant Growth Regulators (PGRs) The production of phytohormones is one of the direct plant growth promotion mechanisms by which a diverse number of bacterial and fungal microbes secrete plant growth regulators and phytohormones including auxins, cytokinins, gibberellins, ethylene, and abscisic acids (Glick 1995; Mukherjee et al. 2018). When these hormones are applied to plants, they increase the root surface area (Vessey 2003). Among all these phytohormones, most of the research has been occurring on the auxin (indole-3-acetic acid) (IAA) (Glick 1995; Verma et al. 2013, 2014) (Fig. 13.1, Table 13.1).

13.4.6.1 Indole-3-Acetic Acid (IAA) Indole-3-acetic acid represents one of the most important plant hormones produced in plant shoot and transported to root (Rashotte et al. 2000) and plays an essential role in plant growth and development in many aspects such as plant cell cycle, cell division, cell enlargement, root initiation, and apical dominance (Vessey 2003). Modulation of these actions by auxin is believed to occur by a change of gene expression of auxin (Guilfoyle et al. 1998). Owing to such desirable modification in plant roots, they can absorb more water and nutrients from the soil, which in turn induces the growth of the plant (Gravel et al. 2007). The role of IAA produced by microbes has received the attention of a number of researchers (Spaepen and Vanderleyden 2011). A diverse number of microbial flora including bacterial and fungal species can produce IAA. On the other hand, some endophytic microbes can also produce IAA (Sessitsch et al. 2004). Two types of pathways determine plant-microbe interactions. If beneficial plant-associated bacteria synthesize IAA, then it follows the indole-3pyruvate pathway, whereas pathogenic bacterial microbes follow the indole-3-acetamide pathway (Patten and Glick 1996; Hardoim et al. 2008). Usually, root elongation is based on the amount of IAA, which could have to regulate plant-microbe interaction. The phytohormone IAA is also taking part in the promotion of symbiosis between legumes and Rhizobium Spaepen et al. (2007) and Molla et al. (2001) found that co-inoculation of Glycine max with A. brasilense and B. japonicum remarkably increases the root surface area, length, number, and dry weight of the root as well as the number and size of root nodules. Some other effects of IAA between plants and phytopathogenic bacteria have also been reported including inhibition of plant growth by disturbing auxin balance in plants resulting in tumors and galls (Jameson et al. 2000; Mole et al. 2007). Based on a recent report, IAA has been found to act as a signaling molecule in several microorganisms, which can affect the gene expression of microorganisms (Prusty et al. 2004; Yuan et al. 2008). There may occur a crucial impact on interactions between IAA-producing microbes. Several research articles have been published that indicate that auxin can act as an effector molecule between auxin-producing microbe-microbe interaction and plant-microbe interaction (Lambrecht et al. 2000; Spaepen et al. 2007; Spaepen and Vanderleyden 2011). Nevertheless, the biological mechanism and role of auxin in fungal ecology have not been widely investigated (Reineke et al. 2008; Rao et al. 2010).

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13.4.6.2 Cytokinin Cytokinins are mostly adenine derivative produced by a number of known microbes such as Azotobacter sp., A. giacomelloi, Agrobacterium sp., A. brasilense, Achromobacter sp., Enterobacter sp., Klebsiella sp., B. japonicum, B. licheniformis, P. fluorescens, and P. polymyxa (Akiyoshi et al. 1987; Cacciari et al. 1989; Taller and Wong 1989; Timmusk et al. 1999; Donderski and Głuchowska, 2000; de García Salamone et al. 2001; Kämpfer et al. 2005; Perrig et al. 2007; Hussain and Hasnain 2009). Cytokinin has the ability to regulate the morphological and physiological processes of plants with the help of differential influence. Cytokinins stimulate cell division, cell cycle, apical dominance, and root hair multiplication, but it also shows lateral root inhibition and inhibits primary root lengthening (Silverman et al. 1998; Riefler et al. 2006). When cytokinin-producing microbes were used as bioinoculant with plants, shoot growth was increased and root to shoot ratio was reduced (Arkhipova et al. 2007). Based on in silico analysis in cytokinin production, it was found that bacterial genes are involved but their role is still not known through functional analyses (Frébort et al. 2011). Therefore, the role of cytokinin produced by PGPR, which influences the root system, remains hypothetical. 13.4.6.3 Gibberellin Kurosawa first isolated gibberellin in 1962 from Fusarium moniliforme. Gibberellins modify plant morphology by elongation and extension of plant roots (Yaxley et al. 2001). Plants, as well as some fungi and bacterial species (Morrone et al. 2009), synthesize gibberellins.Various PGPR produce gibberellins such as A. xylosoxidans, B. cereus, Acinetobacter calcoaceticus, A. lipoferum, A. brasilense, Azotobacter spp., B. pumilus, B. macroides, Herbaspirillum seropedicae, Gluconobacter diazotrophicus, Promicromonospora sp., B. cepacia, and A. diazotrophicus (Bottini et al. 1989; Kang et al. 2009; Bastián et al. 1998; Gutiérrez-Mañero et al. 2001; Bottini et al. 2004; Janzen et al. 1992; Joo et al. 2005; Dodd et al. 2010). Gibberellins produced by plants or microbes facilitate plant modification in various aspects such as stem lengthening, germination, flowering, budding, fruiting, and various other modifications that may be significant for plant growth and its development. 13.4.6.4 Abscisic Acid Abscisic acid is a phytohormone produced by microbes, plants, and animals (Gomez-Cadenas et al. 2015; Karadeniz et al. 2006). Abscisic acid can modulate several aspects of the plant including plant development by stomatal closer (HerreraMedina et al. 2007) and inhibition of the growth of primary roots (Pilet and Chanson 1981). Based on the reports, abscisic acid high in concentration leads to inhibition of the growth of Brassica, beans, and maize (He and Cramer 1996; Cramer and Quarrie 2002).

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13.4.7 Biocontrol Agents In the agriculture system, soilborne pathogenic microbes are the major problem, which hinders agricultural development around the world. Among four groups of pathogenic soil microbes, fungi and nematodes are the major candidates that cause diseases in plants, whereas some bacterial genera are reported to cause diseases in plants (Raaijmakers et al. 2009). Several techniques have been implemented in the agricultural system to enhance crop productivity through better plant nutrition and to protect crop plants from a range of pathogenic microbes. These approaches for agricultural development include the use of organic manures, chemical pesticides, cultivation techniques, compost, and other techniques (Whipps and Gerhardson 2007). At present, chemical fertilizers and manipulated resistant varieties are the most popular measures to protect plants from pathogens (Vassilev et al. 2006). Many biocontrol agents have been isolated that reduce the risk or severity of plant diseases. For example, Pseudomonas, Bacillus species, and Trichoderma species act as biocontrol agents showing excellent antipathogenic activity (Gerhardson 2002). Some bacterial endophytes are also reported to show biocontrol activity against a wide range of fungal pathogens (Berg and Hallmann 2006; Chouhan et al. 2021c). Many PGPR have been identified that show antagonistic activity through several mechanisms such as the production of antibiotics, enzymes, siderophore, and HCN (Podile and Kishore 2006). Diverse PGPR can produce some specific peptide hormone that inhibits the synthesis of cell wall and cell membrane structure and hinders the formation of protein in microbes (Maksimov et al. 2011). Many bacterial species have been identified that produce antibiotics, for example, Pseudomonas spp. and the other bacterial species such as Stenotrophomonas Bacillus, Streptomyces secrets zwittermicin A, xanthobaccin, oligomycin A, and kanosamine, which secrete phenazine, hydrogen cyanide, amphisin, 2,4-diacetyl phloroglucinol, and cyclic lipopeptides (Compant et al. 2005).

13.5

PGPR for Stress Management

Plant growth-promoting rhizobacteria have also been shown to possess properties for the management of different abiotic stresses in plants. They have been proved to be beneficial in stresses such as salinity stress, drought stress, acidity stress, nutrient deficiency, suboptimal root zone temperature, heavy metal stress, and also different biotic stresses. For instance, salinity stress in plants is ameliorated by PGPR by ACC (aminocyclopropane-1-carboxylate) deaminase and ROS (reactive oxygen species) scavenging enzyme activities (Bharti and Barnwal 2019; Vaishnav et al. 2016; Mishra et al. 2018). Under salinity stress conditions, PGPR produce ACC deaminase, osmolytes, antioxidants, and other secondary metabolites that help the plant in coping with stress conditions (Babar et al. 2021). The current strategy for the management of abiotic stress conditions is the isolation of salinity-tolerant PGPR from the rhizosphere of a plant followed by its exogenous application in the rhizosphere of an identified abiotically stressed soil. Drought stress in plants is

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mitigated by PGPR through the modulation of IAA, ABA, ethylene, and various other plant hormones inside the plant tissues under drought stress conditions (Desoky et al. 2020). The regulation of plant hormone levels helps in the enhancement of root and shoot growth, thereby ameliorating the negative effects of drought stress. The production of osmoprotectants also aids in combating drought stress.

13.6

Future Perspective and Challenges

Plant growth-promoting rhizobacteria have been greatly used in the enhancement of plant growth and development. They have also shown great significance in the management of abiotic and biotic stresses. Further, the importance of PGPR in recent times has been realized for the degradation of xenobiotic compounds for potential bioremediation. Different aspects of PGPR with respect to beneficial effects on plants need to be explored. The deleterious effects of weed can be minimized along with the enhancement of plant growth promotion and development by the exploitation of PGPR along with rhizobia. The complex interactions between PGPR microbes need to be studied more deeply to understand the mechanisms behind such interactions. This could help explore more dimensions in the study of PGPR interactions with the plants for growth and development. A deeper look into the genetics of root colonization along with the molecular interactions of plant microbial signaling may help better understand the mechanisms behind plant growth promotion and development.

13.7

Conclusions

PGPR aid plants in their growth and development even in adverse conditions by modulation of soil chemistry and regulating various parameters involved in it. These can be both symbiotic and nonsymbiotic depending upon their relationship with their interacting host plant but one thing is for sure they help release various plant hormones and secondary metabolites that aid the growth and development of various plant parameters. PGPR also help in the mitigation of various stresses by secretion of different secondary metabolites. Apart from their use in plant growth and development, PGPR have also been shown to play an important role in the bioremediation of various heavy metals and side by side aiding in plant growth and development. Their biocontrol properties in the management of various weeds and pests also add to the list of beneficial properties possessed by PGPR. PGPR can be used as effective biofertilizers for enhancing sustainable agricultural productivity. These microbial inoculants will be cost-effective, environmentally friendly, and economically viable. In the future, this seems to be the best alternative to chemicals in farming. Acknowledgments The authors are thankful to Science and Engineering Research Board (SERB), (EEQ/2021/001083) and DST (DST/INT/SL/P-31/2021; DST/SEED/SCSP/STI/2020/426/G) and

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Banaras Hindu Univeristy-IoE (6031)-incentive grant for financial assistance for research work related to research and development of endophytes and plant-microbe interaction.

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Rhizosphere Engineering for Systemic Resistance/Tolerance to Biotic and Abiotic Stress

14

Jyotsana Tilgam, N. Sreeshma, Parichita Priyadarshini, R. K. Bhavyasree, Sharani Choudhury, Alka Bharati, and Mushineni Ashajyothi

Abstract

In the wake of climate change and global warming, plants are continuously confronting environmental stress. Environmental stress inexhaustibly impacts plant productivity and sustainability worldwide. The engineering of the rhizosphere could be an option to alleviate both biotic and abiotic environmental stresses. The rhizosphere is the soil–root interface that encompasses a dynamic physical, chemical, and biological ambiance, favoring varied micro-organisms activity. The microbiome of the rhizosphere influences the plant nutrition, root architecture, and soil quality. The rhizosphere microbiomes have intrinsic metabolic and genetic capabilities in regulating plant stress responses too. The knowledge of the rhizosphere and its components is necessary to create strategies for contouring the rhizosphere to enhance plant fitness and productivity. The advancement of meta-omics technologies and bioinformatics tools have unveiled

J. Tilgam (*) ICAR-National Bureau of Agriculturally Important Microorganisms, Mau, Uttar Pradesh, India ICAR-National Institute for Plant Biotechnology, Indian Agricultural Research Institute, New Delhi, India N. Sreeshma · S. Choudhury ICAR-National Institute for Plant Biotechnology, Indian Agricultural Research Institute, New Delhi, India P. Priyadarshini ICAR-Crop Improvement Division, Indian Grassland and Fodder Research Institute, Jhansi, Uttar Pradesh, India R. K. Bhavyasree ICAR-Regional Research Station, Punjab Agriculture University, Gurdaspur, Punjab, India A. Bharati · M. Ashajyothi ICAR-Central Agroforestry Research Institute, Jhansi, Uttar Pradesh, India # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2022 U. B. Singh et al. (eds.), Re-visiting the Rhizosphere Eco-system for Agricultural Sustainability, Rhizosphere Biology, https://doi.org/10.1007/978-981-19-4101-6_14

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the organization, function and dynamics of the rhizoshphere microbiome of diverse environments. The scientists and researchers are more focused on reshaping the rhizosphere using breeding, biotechnological tools, or supplementing with microbial inoculants, etc. This chapter deals with the various strategies of rhizosphere engineering for the alleviation of abiotic and biotic stress to plants.

14.1

Introduction

In the twentieth century, the green revolution bestowed the world with remarkable gain in food production owing to the use of chemical inputs, high-yielding varieties, etc. However, the enhanced use of chemicals caused a detrimental impact on environmental health. Moreover, climate change and climate-related scourges have aggravated their negative impact on plant productivity and sustainability worldwide (Pachauri et al. 2014). The scenario of climate change created an immediacy to look for the new revolution in agriculture to sustain the food, feed, and fiber requirements of the ever-growing population. The new revolution is possibly including a bio-revolution based on the application of biological inputs (e.g., bio-inoculants, the product thereof) and improved varieties (targeting the microbiome community structure) (Timmusk et al. 2017; Backer et al. 2018). The bio-revolution concept is centered on the manipulation of the rhizosphere by various means. Hence, an in-depth understanding of the rhizosphere and its components is essential to generate strategies for reshaping the rhizosphere to enhance plant fitness and productivity. The omics technology and molecular tools are continuously unveiling the mystery of the rhizosphere. The organization, function, and dynamics of rhizosphere microbiome have been explored by researchers in a diverse environment.

14.1.1 An Insight into the Rhizosphere and Its Components The rhizosphere is the confined zone of contact between plant roots and soil particles, inhabited by a diverse group of micro-organisms (Dessaux et al. 2016; Ahkami et al. 2017). McNear Jr (2013) has illustrated the rhizosphere as having three regions: the endorhizosphere, rhizoplane, and ectorhizosphere (Fig. 14.1). Endorhizosphere is the section of the root cortex and endodermis in which the apoplastic spaces harbor microbes and mineral ions. The rhizoplane is the central region beside the root epidermal cells and mucilage. The ectorhizosphere is the outermost zone which extends from the rhizoplane out into the bulk soil. Plant metabolism greatly influences the rhizosphere by releasing metabolites (root exudates), plant debris (dead cells, mucilage), and carbon dioxide (Dessaux et al. 2016; Ahkami et al. 2017) that assist different and distinctive patterns of microbial colonization. This plant root–soil interface creates a dynamic physical, chemical, and biological ambiance for micro-organisms to perform inter- and intra-species

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Rhizosphere Root Rhizoplane

Root Hairs

Endorhizosphere Ectrohizosphere Vascular tissues

Mucigel (Plant and microbes mucilage) Epidermis

Root cortex Endodermis

Bulk soil Root cap

Sloughed root cap cells

Fig. 14.1 A simplified diagram of rhizosphere region

communication. The microbiome of the rhizosphere plays pivotal roles in soil formation, acquisition of nutrients, suppressing pathogen pressure, secretion and modulation of extracellular compounds like secondary metabolites, hormones, signaling molecules, antibiotics, etc. favoring plant growth promotion and protection. Bacteria, fungi, archaea, and arbuscular mycorrhizal fungi (AMF) are prevalent micro-organisms that help in the nutrition recycling process (Van Der Heijden et al. 2008). The microbiome of rhizosphere is also known for plant protection using various mechanisms for disease suppression, and also salinity and drought stress alleviation, etc. However, the rhizosphere zone is more vulnerable to environmental stress. It is found that the salinity stress in the rhizosphere reduces the survivability of plants (Damodaran and Mishra 2016).

14.2

Rhizosphere Engineering and Different Approaches

The biochemistry of soil and root interface is the effect of various interacting and competing processes based on plant physiology, soil type and water content and microbiome composition (Pinton et al. 2007). For the betterment of plant fitness and productivity, the entire rhizosphere component can be engineered. Till now, research has presented that rhizosphere can be engineered by proper selection of crop genotype, by application of microorganisms or soil amendments, and by genetic

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manipulation of plant and microbiome activities. Application of microbes or soil amendments improves soil quality via changing its physicochemical properties (Dessaux et al. 2016). Plants can be engineered to select or introduce beneficial and novel traits such as the rhizosphere pH or to release compounds that improve nutrient availability, protect against biotic and abiotic stresses, or encourage the proliferation of beneficial microorganisms (Bowen and Rovira 1999; Damodaran and Mishra 2016). Currently, for microbiome engineering, the whole microbial population (present in plant and rhizosphere) instead of single strain engineering are selected to stimulate plant growth promotion and protection. Similarly, the emergence of “omics” approaches has unraveled the molecular basis of plant– microbe interaction mechanisms responsible for the physiological changes. Hence, engineering of plant–microbe interaction (holobiome approaches/ecological engineering) like an exciting strategy came into the picture. In the coming section, engineering strategies and relevant instances are explained in detail.

14.2.1 Soil Amendments Rhizosphere is the soil compartment around the roots that influence the root activity and plant growth. The physical and chemical properties of the rhizosphere depend on the soil type, water content, soil microbes as well as the biological activities of the plants (Ryan et al. 2009). So, engineering any of these factors will help us tailor the rhizosphere thereby influencing the biogeochemical activities in the root zone. The microbiome present in the root zone is diverse with both beneficial and pathogenic microbes which regulate the nutrient dynamics as well as the wellbeing of the crop plants. So rather than increasing the nutrient concentration through fertilization, it is wiser to go for efficient root zone management approaches utilizing the hidden potential of the root zone. The amendments can be done by modifying the physical and chemical properties of the soil in the root zone. These properties of soil are a function of the percentage of clay, nutrient status, organic matter, and the water-holding capacity (Bowen and Rovira 1999). The soil is a substrate that determines the survival rate as well as the growth of several microbes. Several studies suggest that the clay particle could promote microbial growth as it plays an important role in determining the waterholding capacity and the pore size of the soil bulk. It promotes the useful microflora by adsorbing inhibitory substances as well as conferring desiccation tolerance to the cells. The soil moisture will affect the survival of different microorganisms, especially fungi. The bacteria are more desiccation-tolerant due to their ability to produce spores. The pores in the clay particles can also provide physical protection of the microflora against their predators. The soil temperature is another factor which affects the rhizosphere and an increase in temperature reduces the antagonistic microbes but it also affects the growth of beneficial ones (Moyano et al. 2007). It is found that physical processes like tillage generally reduce the microbial count by destroying the vegetative propagules of microbes, especially some useful fungi. But the tillage practices like

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conservative tillage will help improve the growth and colonization of microbes as well as the physical properties of soil (Mirás-Avalos et al. 2011; Wang et al. 2017, 2020). The nutrient availability in agroecosystems has resulted from the interaction between fertility management strategies and the microbial processes including biological nutrient fixation and mineral mobilization (Schmidt et al. 2019). So, another approach is to influence the plant root architecture by altering the soil nutrient status. The intensity of soil nutrients can affect the root proliferation which decides the adsorption area of the roots. An optimum supply of soil nutrients in the initial phase of crop growth will help to develop an extensive root system. Also, it will affect the growth of beneficial rhizosphere microbes like nitrogen-fixing bacteria and phosphate-solubilizing bacteria. The site-specific application of the nutrients like N and P can encourage root proliferation which can result in enhanced growth, biomass and nutrient absorption rates (Kumar et al. 2017). The strategic nutrient supply can be adopted to stimulate the root growth, to exploit the rootmobilizing potential, and to delay the root senescence (Shen et al. 2013). The application of synthetic fertilizers also alters the pH of the soil thereby affecting the rhizosphere activities. The use of nitrogenous fertilizers usually lowers the soil pH. This can increase the growth of acidobacteria and decrease the abundance of beneficial ammonia-oxidizing archaea. The deficiency of the nutrients like Zinc and Manganese will make the plants susceptible to some soil pathogens (Bowen and Rovira 1999; Schmidt et al. 2019). Even though the agrochemicals like herbicides can destroy the plant pathogenic rhizosphere microflora, they detrimentally affect the colonization of beneficial ones (Bowen and Rovira 1999). The major energy source of the rhizosphere microbiome of a specific crop is the plant organic matter and the microbial colonies in the root residues act as the inoculum for the successive crops. So, the addition of plant organic matter is one of the methods to alter the microbial diversity in the rhizosphere (Bowen and Rovira 1999). The addition of organic fertilizers such as composts and crop residues can alter the diversity, abundance, and activity of various soil microbes, especially the nitrogen-fixing bacteria (Schmidt et al. 2019). Biofertilizers containing different types of plant growth regulating rhizobacteria and fungi can drastically change the rhizosphere microbiome status as well as the nutrient availability in the rhizosphere. The combination of organic fertilizers, effective microorganisms, and biofertilizers is proved to be the most efficient way to engineer the rhizosphere through soil amendments without compromising environmental safety (Jilani et al. 2007).

14.2.2 Plant as a Management Tool The plant roots are the complex resource-rich hotspots that can selectively control the microflora in the rhizosphere which is different from the bulk soil. So, for a longterm improvement of the rhizosphere, the improvement of plant itself through conventional or using biotechnological methods is inevitable. This can be done by influencing the root itself or by influencing the rhizosphere microbiome by selective

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Table 14.1 Genes responsible for the root system architecture traits for important crops Crop Rice

Gene OsPIN2 DRO1 OsEXPA8

VRN1

Phenotype/traits associated Large root angle Deeper rooting Longer primary roots, more lateral roots and root hairs Root hair formation Lateral root formation, root length, phosphate and arsenate accumulation Root system architecture in low nitrogen availability Root length and root angle

TaMOR qSRA-6A

Number of roots Seminal root angle

ZmRAP2.7 ZmTIP1 ZmPTF1

Brace root development Root elongation Root development and drought stress signaling Root hair growth Increased root biomass under water stress

OsEXPB2 OsWRKY28 RDWN6XB Wheat

Maize

LRL5 LOS5/ ABA3 AtLOS5 ZmbZIP4 Barley

VRN1

Soybean

BetaExpansin GmEXP1

Root ion fluxes under salt stresses Lateral and primary root development during stress Root length and root angle Root hair formation Root elongation

Reference Wang et al. (2018) Uga et al. (2013) Ma et al. (2013) Zou et al. (2015) Zhao (2018) Anis et al. (2019) Voss-Fels et al. (2018) Li et al. (2016) Alahmad et al. (2019) Li et al. (2019a) Zhang et al. (2020) Li et al. (2019b) Wang et al. (2019) Mohammed et al. (2019) Zhang et al. (2012) Ma et al. (2018) Voss-Fels et al. (2018) Kwasniewski and Szarejko (2006) Lee et al. (2003)

modification of rhizodeposition (organic and inorganic compounds released by roots) (Ryan et al. 2009). The root system architecture (RSA) of the plant is an important factor that determines the rhizosphere environment. So many genes are associated with the processes that determine this complex trait in different plants (Table 14.1). Several component traits contribute to RSA and thus the rhizosphere which includes the root depth, root hairs, primary and lateral root number, root angle, etc. The degree of root penetrations differs according to the genotype which determines not only the soil physical properties in the rhizosphere but also the degree of root–soil contact and hence the nutrient availability (Gregory et al. 2013). Due to the difficulties in the phenotyping techniques of these traits, the studies are limited and in the developing stage. The plant roots harbor several genes controlling nutrient fixation processes. These genes could increase the nutrient use efficiency and reduce the demand for chemical

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fertilizers. These genes will interact with useful microbes like nitrogen-fixing bacteria, phosphate-solubilizing bacteria, vascular arbuscular mycorrhizae, archaea, etc. and stimulate their colonization and growth. The genes like the N transformationassociated genes will interact with the soil microbiome and provide a specific rhizosphere ecosystem. The maize genes like nifH (nitrogen fixation), gdh, ureC (ammonification), amoA, hao (nitrification), and narG, nirS/nirK, norB, nosZ (denitrification) are examples for this (Schmidt et al. 2019). The researchers are also aiming to increase the P-acquiring ability of the plants from common forms of soil organic phosphates. As a result, transgenic plants with microbial phytase genes have been developed and they can hydrolyze P from inositol phosphates with 20-folds increase in root phytase activity (Gregory et al. 2013). The rhizosphere compositions of plants are controlled by the organic materials around the roots which include exudates, secretions, lysates, and plant mucilages. The exudates and secretions are the compounds released by the roots and promote the growth of beneficial microbes. The lysates are the compounds released from senescent or ageing cells, which help the plant to control the pathogenic microbes (Rovira et al. 1978). The mucilage is a gelatinous polysaccharide produced by the root cap which helps roots in penetration. The composition of the root mucilage varies according to the species and genotype of the plant. For example, the rice and the maize mucilages are rich in fructose while the grasses in the Lolium spp. contain glucose and xylose. The composition of mucilage will affect the rhizosphere by influencing the biological, viscoelastic, and surface tension properties of soil (Gregory et al. 2013). This rhizodeposition will, directly and indirectly, affect the rhizosphere composition as well as the rhizosphere microbiome. So, engineering the plant genes responsible for these compounds is another way of rhizosphere engineering. The unexplored area of root biology can be explored with novel phenotypic techniques. Then these traits can be engineered by using conventional plant breeding approaches coupled with novel biotechnological tools.

14.2.3 Microbe Engineering Engineering of microbe community responsible for plant growth, biotic and abiotic stress resistance, and nutrient mobilization for rhizosphere presents a unique opportunity for enhancing crop performance. Microbe cortege surrounding plant root system has been studied for its direct and indirect interactions. For rhizosphere engineering, PGPM are of particular interest. These growth-promoting bacteria directly benefit plants by (1) mobilizing and fixing nutrients, (2) Modulating plant growth by interacting plant growth hormones, and indirectly by (1) Efficient root colonization, (2) Biopesticidal and biocontrol activities, and induction of defense mechanism by SAR (Tailor and Joshi 2014). Most of the studies focused on selecting an effective combination of plant growth-promoting rhizobacteria (PGPR) for inoculating rhizosphere and only a few reports explain the engineering of PGPR for its effective use (Raaijmakers et al. 1995). Introduced heterologous siderophore in Pseudomonas spp. confer a competitive advantage in interactions in

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the rhizosphere. Many studies have been done where microbes are engineered to improve nodulation efficiency of plant, for example, Sinorhizobium meliloti strain constitutively expressing putA gene resulted in increased activity of proline dehydrogenase, an enzyme crucial for colonization. Better colonization of engineered strain resulted in better nodulation in alfalfa roots (Van Dillewijn et al. 2001). Introduction of ACC deaminase structural gene (acdS) and its upstream regulatory gene lrpL, from R. leguminosarum bv. viciae 128C53K in Sinorhizobium meliloti also increased nodulation efficiency of alfalfa (Ma et al. 2004). Similarly, overexpression of trehalose-6-phosphate synthase in Rhizobium etli improved nodulation, drought tolerance, and yield in Phaseolus vulgaris (Suárez et al. 2008). Several cryptogamic diseases got suppressed when the soil was inoculated with genetically modified Burkholderia vietnamiensis PGPR strain P418. This engineered strain having chitinase from Bacillus subtilis leads to suppression of wheat sheath blight, cotton Fusarium wilt, and tomato grey mold (Zhang et al. 2012). The transgenic strain of Ensifermedicae MA11 carrying copAB genes from a Cu-resistant Pseudomonas fluorescens strain is able to alleviate Cu tolerance in Medicago truncatula in Cu-contaminated soil and successfully forming nodules (Delgadillo et al. 2015). Population engineering rather than single microbe engineering is a novel aspect but ecological interaction among microbes also needs to be considered (Großkopf and Soyer 2014). Types of ecological interactions are commensalism, competition, predation, no interaction, cooperation, and amensalism. Our goal of maximizing beneficial interaction and minimizing negative interaction is particularly challenging as negative interaction tends to dominate the event in two strain co-culture (Foster and Bell 2012). Vast knowledge about naturally occurring PGP microbes that colonize rhizosphere is available in the public domain. Some of these genera like Pseudomonas, Bacillus, Paenibacillus, Streptomyces, Rhizobium have genome sequences available and genetic systems amenable for engineering (Rothmel et al. 1991; Dong and Zhang 2014; Kim and Timmusk 2013; Medema et al. 2011; Patel and Sinha 2011). For making a synthetic community of microbes most suitable species will be Bacillus as its sequencing information is available in higher depth, transformation is relatively easy (Dong and Zhang 2014), many isolates having plant growth property (Köberl et al. 2013, 2015), and also used as a biocontrol agent. Bacillus species are broad-spectrum antagonists to the soil-borne pathogen (Köberl et al. 2013) hence different antibiotic-producing pathways from different strains may be clubbed together to form a synthetic strain. Bacillus spp. could be engineered for producing a high concentration of hormones or for nitrogen-fixing machinery (Arkhipova et al. 2005; Kim and Timmusk 2013). These engineered bacillus strains could be combined with some naturally occurring nitrogen fixer from Rhizobium and/or Bradyrhizobium genera to generate consortium (Ahkami et al. 2017). For increasing cooperation among microbes of synthetic community, strains should be engineered in such a manner that each species would depend on cofactor produced by other species for survival. In this way symbiotic relationship between different synthetic species will develop and competition will be eliminated. Some factors which must be considered for selecting microbe for engineering rhizosphere are:

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(1) colonization efficiency of microbe in root surface, rhizosphere, and target host plant; (2) its survival and competition with other microbes in consortia; (3) attachment to the root surface; (4) its plant growth-promoting activity and relation with other PGPR microbial species; (5) abiotic stress tolerance; (6) density of growth; (7) tolerance to herbicides, pesticides, and fertilizers.

14.2.4 Plant–Microbes Interaction Engineering The profile of rhizospheric microbes in rhizosphere depends on the rhizospheric deposition. Substrate from root exudates determines establishment of host-specific microbe community in rhizosphere. So, genotype of plant and rhizospheric microorganism profile is very fine-tuned. 5–21% of photosynthetically fixed carbon are secreted in root exudates in the form of different metabolites (Bais et al. 2006; Zhang et al. 2015). For plant–microbe interaction, phytohormone plays an important role. Many PGPR microbes are known to be producing phytohormone, including auxin, gibberellin, cytokinin. Other than these, inoculation with nonpathogenic microbes also induces cross-talk between jasmonic acid, salicylic acid, and ethylene to induce systemic acquired resistance (SAR) and induce systemic resistance (ISR), which further protect plants from pathogenic microbes. Plant–microbe interaction engineering is an exciting field of study which also involves plant engineering strategies concerning the plant immune system and mainly focuses on phytohormone pathways and crosstalks. Several studies related to endophyte and phytoremediation are already present, for example, endophytic bacterium Burkholderia cepacia engineered for toluene degradation pathway by adding pTOM toluene-degradation plasmid improves toluene degradation capacity of lupine. Lupine seeds when inoculated with this engineered bacterium resulted in reduced phytotoxicity and 50–70% reduction in leaf evapotranspiration. This kind of engineered plant–microbe association is promising in improving the efficiency of phytoremediation volatile organic contaminants (Barac et al. 2004). In another experiment, poplar hybrids (P. trichocarpa X P. deltoides) were inoculated with Burkholderia cepacia VM1468 carrying Toulene degrading plasmid pTOM-Bu61. Control plants were treated with soil bacterium B. cepacia Bu61 (pTOM-Bu61). The treatment plant showed positive growth in presence of toluene and reduced evapotranspiration of toluene. An interesting result of this experiment was that Burkholderia cepacia did not form endophytic relationship with poplar. Indeed, toluene tolerance resulted from horizontal gene transfer to endogenous bacteria of endophytic community (Taghavi et al. 2005). These kinds of in planta horizontal gene transfer among plant-associated endophytic bacteria could be used to change natural endophytic microbial communities for phytoremediation. Endophytic bacterial isolates of eggplant, cucumber, and groundnut mainly (more than 50%) consisting of Pseudomonas fluorescens reduced the incidence of wilt and damping-off caused by Ralstonia solanacearum. Most of the selected antagonists produced an antibiotic, DAPG, which inhibited R. solanacearum in vitro (Ramesh et al. 2009). Several studies on plant endophyte interaction in relation to phytoremediation and PGPR have been

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done. Major difficulties in these cases are maintaining the desired level of microbial population in the rhizosphere. The rhizosphere is influenced by many environmental and edaphic factors. Also, microbial population depends upon genotype of the plant. So, for maintaining the desired level of microbes in the root zone of the plant engineering for root exudates is the proposed idea. This idea is based on opine production in Agrobacterium infected plant (Tempe and Petit 1982). Opines are low molecular weight compounds used as a carbon source by Agrobacterium. Agrobacterium transfers a TDNA containing opine synthesis gene present in their plasmid to the plant genome which results in opine production in plant roots. These opines are secreted by plant roots gall and facilitate Agrobacterium growth. Based on this concept, some studies have been conducted where plants are transformed to produce opines that facilitate growth of indigenous or introduced opine-degrading enzymes. These methods showed their independence from the plant species and soil but nature and concentration of opine lead to the selection of different profiles of indigenous microbes (Tempe et al. 1982; Murphy et al. 1987; Oger et al. 2004; Mondy et al. 2014). To maintain a sufficient level of microbes, engineering trophic link is a promising approach, a natural example of which is nodulating N fixing bacteria. The bacteroids formed in nitrogen-fixing nodules synthesize opine-like compounds that specifically favor the growth of free-living bacteria. In Arabidopsis root was modified after foliar application of flagellar peptide flg22 or coronatine, a bacterial toxin. Application of these compounds increased the expression of malic acid transporter AML1 leading to increased concentration of malic acid in the root zone. Increased malic acid favored PGPR Bacillus subtilis strain FB1A7 and induced systemic resistance response in plants against P. syringae pv. tomato (Lakshmanan et al. 2012). Plant–microbe interaction research can be accelerated by combining metagenomics metabolomics and culture-dependent synthetic communities (SynComs) approach (Liu et al. 2020). Metagenomics will be helpful in determining the structure and function of microbial profile in the rhizosphere followed by culture of microbes to form SynComs. These Syncom axenic plants are manipulated. Plant growth properties of Syncom can be studied using metabolomic approach. Change in plant interacting microbial profile due to environmental stress will be better understood by utilizing all the above approaches.

14.3

3Rhizosphere Engineering to Confer Abiotic Stress Tolerance to Plants

14.3.1 Temperature Extreme High temperature/heat stress is one of the most challenging environmental risks for plant growth and development. Heat stress causes severe cellular disorganization, denaturation, and aggregation of cellular proteins ultimately leading to cell death. To survive this stress, plants develop multiple strategies which are achieved by the regulation of heat stress-induced genes. Adopting plant breeding and genome editing

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strategies are widely followed approaches for developing heat-tolerant crop cultivars but each strategy has its own drawbacks. Plant breeding programs are very timeconsuming and depend on the availability of diverse germplasm. Strategies like transgenics and gene/genome editing technology requires the identification of the candidate genes which is quite complicated and costly. Additionally, the adoption rate of this technology is quite low due to biosafety issues. An alternative and cheap approach for attaining heat stress tolerance in plants can be the exploitation of soil microbes that positively interact with the plant system. Certain soil-inhabiting bacteria like plant growth-promoting rhizobacteria (PGPR) isolates have been identified that accelerate plant growth under heat stress. For example, treatment of wheat seeds with Bacillus amyloliquefaciens UCMB5113 or Azospirillum brasilense NO40 resulted in improved heat stress tolerance in wheat (Abd El-Daim et al. 2014). In another study, Bacillus cereus was assessed for plant growth-promoting activities under heat stress conditions in tomato varieties. The control plants were drastically affected by heat stress while bacterial inoculation promoted different morphological traits like positive shoot and root growth, increase in fresh and dry weight (Mukhtar et al. 2020). These instances suggest that PGPR are good candidates for improving crop productivity and imparting heat stress tolerance in crops. Fungal endophytes have also been reported to play a significant role in plant survival under various abiotic stress conditions such as drought, salinity, extreme temperature (cold/ heat), heavy metal pollution, etc. (Singh et al. 2011). Chilling/freezing temperature causes plant cells to expand as the water inside them turns to ice which can rupture and lead to cell death. The effect of cold temperature on plant system is alleviated by activating various metabolic pathways via activation of large arrays of transcription factors. As in heat stress, there are also reports of various microbes which are known to impart cold tolerance in crops. For example, grapevine plants inoculated with Bacillus phytofirmans strain PsJN accumulated higher levels of carbohydrates, proline, phenols, and showed elevated rates of photosynthesis and starch deposition compared to control plants during cold stress (Barka et al. 2006). Moreover, inoculation of grapevine with the same PGPR strain lowered the rate of biomass reduction and electrolyte leakage (an indicator of cell membrane injury) during cold treatment at 4  C, and also promoted post-chilling recovery. Table 14.2 enlists a few experimental evidences for the role of microbial symbionts in plant response to chilling/freezing stresses (Acuña-Rodríguez et al. 2020). Studies suggest that priming of these beneficial microbes with plants enhances/ stimulates induced systemic resistance which facilitates abiotic stress (heat) tolerance in various crops. Therefore, rhizosphere engineering is a feasible option for developing heat stress tolerant cultivars which can be accomplished either by redesigning the plant metabolism or introduction of synthetic microbial communities into the rhizosphere.

14.3.1.1 Redesigning the Plant Metabolism Plant root exudates act as chemoattractants for the rhizospheric microbial communities and it has been recently reported that variation in the composition of

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Table 14.2 Experimental evidences for the role of microbial symbionts in plant response to chilling/freezing stresses (Acuña-Rodríguez et al. 2020) Plant tissue Roots

Host species Solanum lycopersicum (crop— herbaceous)

Symbiont Pseudomonas vancouverensis and P. fredericksbergensis (bacteria)

O. sativa (crop— graminoid)

B. amyloliquefaciens, Brevibacillus laterosporus (bacteria) G. mosseae (AMF)

Roots

R. irregularis (AMF)

Roots

S. lycopersicum (crop— herbaceous)

Trichoderma harzianum (fungus)

Seeds

H. vulgare (crop— graminoid)

Glomus versiforme, R. irregularis (AMF)

Roots

C. sativus (crop— gourd)

R. irregularis (AMF)

Roots

Vaccinium ashei and V. corymbosum (crop—shrub) C. sativus (crop gourd)

Roots

Salient findings B+ tomato plants showed high chilling tolerance under chilling stress (10–12  C), showed lesser cell membrane damage and ROS concentrations, which might be due to the expression of cold acclimation genes (LeCBF1 and LeCBF3) B+ plants showed higher proline and chlorophyll concentrations than B- plants under cold stress (0–5  C) AMF inoculation increased leaf antioxidant activity under cold stress (10  C) Large array of genes were upregulated in AMF inoculated plants and down-regulated in non-AMF plants under cold stress (13  C) E+ plants under cold stress (8  C) exhibited improved photochemical PS II efficiency, growth, electrolyte retention and proline concentration as compared to E- plants Improved plant growth, photosynthesis, phosphorus uptake and osmotic regulation at 5 and 25  C, and enhanced post freezing survival at 5  C The AMF enhanced plant photosynthetic efficiency at lower temperature. This enhancement might be due to the higher carbonsink strength observed on AMF-inoculated plants

B-, not bacterized; B+, bacterized; E-, endophyte-free; E+, endophyte-inoculated

root exudates can change the preference for different microbial community assemblages and functions (Sasse et al. 2018). For example, foliar application of jasmonic acid changes the chemical composition of the root exudate and thereby the rhizosphere microbiome community composition in Arabidopsis (Doornbos et al. 2011; Carvalhais et al. 2013). Abiotic stress environment can modify root exudation patterns through various mechanisms and genes involved in these mechanisms mostly belong to ABC family and MATE family (Zhou et al. 2019). Augmented exudation rate has been evident under abiotic stress environment with the release of

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primary and secondary metabolites to the rhizosphere when plants are subjected to drought, high salinity heat stress Al-toxicity, or Pb-toxicity and flooding. All these metabolites can attract the microbiota which will help in establishing mutualistic relationships between plants and plant growth promoting rhizobacteria or mycorrhizal fungi (Vives-Peris et al. 2020). This positive interaction can induce a variety of benefits for the plants through different mechanisms, including production of phytohormones, siderophore production, biofilm formation, fixation of atmospheric N, etc. (Etesami and Glick 2020). Since many genes-controlling exudates have been identified, it is possible to genetically modify plants to redesign the rhizosphere for desired features. However, it is important to consider that redesigning plant to influence rhizosphere could be a very complex process due to little knowledge about exudates composition, degradation of the engineered compound in the soil, low exudation rate, the effect of plant development, and external stimuli on exudation time and levels. Thus, advances in understanding the plant– microbe interaction in the rhizosphere are necessary for the development of improved genotypes for improved sensitivity to the application of specific microbial inoculants (Schlaeppi and Bulgarelli 2015).

14.3.1.2 Introduction of Synthetic Microbial Communities Building up synthetic microbial communities to impact rhizosphere requires vast knowledge about the naturally occurring microbiota. Many microbial genera are known that colonize the rhizosphere, have publically available genome sequences, and are amenable to genetic engineering efforts. These genera include Pseudomonas, Paenibacillus, Bacillus, Streptomyces, and Rhizobium (Abd El-Daim et al. 2014). However, designing artificial microbial communities represents a huge challenge and raises many questions which need to be answered first. There are many types of ecological interactions that operate between microbial strains. The interactions can be positive (cooperation, commensalism, mutualism), negative (ammensalism, competition, and predation), or no interaction and the complexity of these probable interactions will scale linearly with the addition of extra strains (Großkopf and Soyer 2014). The main challenge in this approach is to minimize parasitism and competition and maximize cooperation. Minimizing competition is particularly challenging as even in two strain co-cultures competition tends to dominate rather quickly (Foster and Bell 2012). Further, environmental factors, such as root exudates, pH, temperature, nutrient availability, also affect stabilization, growth rates, susceptibility to pathogens, and sustainability of the applied synthetic microbial community. PGPR have been reported to alleviate extreme temperature effects in various crops and promoted growth under stressful environments (Abd El-Daim et al. 2014; Mukhtar et al. 2020). Hence, exploiting such PGPR via a multi-omics approach for the development of the synthetic microbial community or as a source for novel genes can be a feasible option for improving crop productivity under the changing climate scenario.

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14.3.2 Drought Global water scarcity is a major threat to agriculture and the changing climate will further aggravate the problem affecting plant growth and development. An impressive number of scientific reports on plant drought tolerance mechanisms are available in the public domain but the complexity of the trait has slowed down the progress in this field. The rhizospheric bacteria coevolved with plant roots play an important role in the coping strategy of plants to drought. PGPR impart drought tolerance in plants by releasing exopolysaccharides, 1-aminocyclopropane-1-carboxylate (ACC) deaminase, volatiles, phytohormones, osmolytes and antioxidants, regulation of stress-induced genes, and alteration in root morphology (Vurukonda et al. 2016). For example, inoculation of wheat seedlings with Bacillus thuringiensis AZP2 and Paenibacillus polymyxa B resulted in significantly higher survival rate of drought-stressed plants and increased photosynthesis and biomass production which was reflected in alteration in volatile profiles and total emission rates (Timmusk et al. 2014). Phenazines are heterocyclic compounds known to inhibit plant diseases and help in biofilm formation (Thomashow and Weller 1988; Maddula et al. 2006). To understand the specific role of phenazines in drought stress tolerance in plants, phenazines producing rhizosphere-colonizing Pseudomonas chlororaphis 30–84 and isogenic derivatives deficient or enhanced in phenazine production and wild type was used to inoculate in wheat seedlings. After 7-day water deficit, seedlings treated with water or by the phenazine mutant showed wilting symptoms whereas seedlings treated with phenazine producers displayed less severe symptoms. After a 7-day recovery period, the survival rate of wheat seedlings treated with phenazineproducing strains was higher as compared to the water control (Mahmoudi et al. 2019). These studies suggest that the use of rhizospheric microbiota can be an important and cheap strategy to alleviate the effects of drought stress in plants. There are evidences which suggest that plants influence rhizospheric microbes to cope with the drought situation. For example, during drought, maize forms symbiotic association with arbuscular mycorrhizal fungi which modulate water loss by downregulating aquaporin-related genes in the root (Quiroga et al. 2017). Furthermore, in trifoliate orange, mycorrhizal root encourages H2O2 efflux to lessen the effect of oxidative damage during drought stress (Huang et al. 2017). There are also reports which suggest that plant exudates can specifically select bacteria to get protection from drought. For example, drought stress in maize increased the malic acid exudation rate (Henry et al. 2007), which is an effective chemoattractant for Bacillus subtilis (Allard-Massicotte et al. 2016). These scientific evidences hint that to cope with drought situations, rhizosphere engineering can be a good option. Rhizosphere can be engineered by (i) redesigning the plant metabolism where root exudates properties can be altered to select for the desired microbial community, (ii) employing synthetic microbial communities consisting of natural or genetically engineered microbes to rhizosphere. However, the knowledge gap regarding the complex communication in the rhizospheric region during drought needs to be addressed first which will further expedite research on rhizosphere engineering.

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14.3.3 Rhizosphere Engineering for Tolerance to Salinity Salinity refers to a high concentration of soluble salts in the soil and or water, with an electrical conductivity (EC) of the range 4– 5'-CGTTAATGCCG~600nucleotides-ATTTGAGGGAATTGCC-3'* Ascomycota > Firmicutes, while in organic soil, it was Proteobacteria > Cyanobacteria > Actinobacteria. A comparative metatranscriptomic approach was used by Hayden et al. (2018) to assess the taxonomic and functional characteristics of the microbiome of the wheat rhizosphere in suppressive and non-suppressive soils to Rhizoctonia solani. The results showed Arthrobacter and Pseudomonas as the dominant taxa in non-suppressive soil, and Stenotrophomonas and Buttiauxella in suppressive soil. In another study, an analysis of the wheat rhizosphere metatranscriptome was performed to unveil the structural and functional microbial communities associated with organic pollutant degradation. The results showed that Proteobacteria, Actinobacteria and Firmicutes were the dominant phyla involved in the degradation of aromatic compounds. The abundance of the transcripts related to aromatic compounds, phenols, biphenyls, benzoates, naphthalene, carbazoles and xenobiotics revealed the profuse degradation competences in the wheat rhizosphere (Singh et al. 2018). A metatranscriptomic study also reveals the effects of climate change on community shifts in the rhizosphere microbiomes. The probable impact of slightly elevated carbon dioxide (eCO2) was assessed on rhizosphere microbiomes of grasslands. The results unveiled the substantial impact of eCO2 on the structural and functional rhizosphere microbiomes of grasslands. Both root-associated and rhizospheric soil microbiomes had significantly higher bacterial abundance with dominant populations of Actinobacteria and Proteobacteria, while a decline in fungi was observed. In addition, abundance of Acidobacteria, Bacteroidetes, Chloroflexi and Planctomycetes was also observed (Bei et al. 2019). Viruses have influence on nearly all the organisms on earth and greatly impact agriculture, the biogeochemical cycle and human health. Nevertheless, the knowledge on RNA viruses is very negligible in environmental perspective, and indeed, very few are reported with respect to their diversity and interactions in soil, where one of the greatest multifaceted microbial systems exists. Metatranscriptomes from four habitats viz. rhizosphere, detritosphere, rhizosphere with root detritus and unamended soil were assembled and analysed. The results showed huge diversity of Narnaviridae and Leviviridae and they have been reported to infect fungi or Proteobacteria, respectively. The viral and host communities were extremely dynamic and deviated on the basis of presence of root litter. When the host cell dies due to a viral infection, the cell carbon gets mobilised in a process of soil carbon cycling (Starr et al. 2019).

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An analysis of the root microbiome of sorghum has shown that the development of the early root microbiome is delayed by drought. This is due to the escalated abundance and function of monoderm bacteria whose outer cell membrane is absent but a thick cell wall is present. These shifts in community composition were correlated with transformed metabolism of plants and the enhanced functions of ATP-binding cassette (ABC) transporter genes of bacteria. A metatranscriptomic analysis of the Arabidopsis thaliana (genotype Pna-10) rhizosphere microbiome unravelled the expression of 81 novel transcripts at various stages of plant development. It was deduced that root-exudates comprising compounds and phytochemicals are being released by plants at different developmental stages, which restructure the rhizosphere microbiome (Haldar and Sengupta 2015). Metatranscriptomics, along with metagenomics, allowed researchers to characterise endophytes from internal tissues of plant in-situ which would help in identification of unique genes that could help in better understanding of significant functions played by microorganisms for plant growth and enhancement of productivity (Maela and Serepa-Dlamini 2020).

24.5

Metatranscriptomics in Bio-Control of Phytopathogens

In the rhizosphere, the plant pathogens tend to develop a parasitic association with plant roots to initiate infection. The pathogen must contest with the rhizosphere inhabitants in order to invade the root tissues for obtaining nutrients. The growth of pathogens is strongly restricted in disease-suppressive soils due to the influence of specific rhizosphere microorganisms (Chapelle et al. 2016). In most of the soils, the disease suppressive is inherent due to their microbiome which is established in soil after many years of high disease incidence. This indicates the requirement for fungal pathogens in soil to activate specific antagonistic microbes or microbial community and thereby exhibiting the suppressiveness. However, the microbes and their mechanisms in most suppressive soils are still not known. Metatranscriptomics plays a major role in getting insights into the active microbes and their traits expressed during fungal invasion into the plant roots. This approach helps reveal the importance of the genes accountable for suppression and could be used to get the complete expression profile of the microbial community. This would unveil the importance of the microbiome in plant-microbe interactions and disease suppression in the rhizosphere (Kothari et al. 2017). The metatranscriptomic investigation of the sugar beet rhizosphere microbiome in disease-suppressive soil displayed significantly higher relative abundance of Burkholderiaceae, Oxalobacteriaceae, Sphingobacteriaceae and Sphingomonadaceae in the rhizosphere after fungal infection. Also, an upregulation of genes associated with stress (ppGpp) were observed in these families. The invasive pathogens induce the stress responses in rhizosphere microbial communities either directly or via the plant. This leads to a shift in microbiome composition along with the induction of antagonistic characters that limit the microbial infection (Chapelle et al. 2016). A comparative metatranscriptomic investigation was performed to understand the taxonomic and functional characteristics of the rhizosphere microbiome in wheat crop grown in

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adjacent fields which are suppressive and non-suppressive to R. solani. The results revealed that suppressive soils had a higher expression of a terpenoid biosynthesis backbone gene (dxs), a polyketide cyclase and several cold shock proteins (csp). Non-suppressive soils exhibited a higher expression of antibiotic genes such as phenazine biosynthesis (phzF), transcriptional activator of phenazine synthesis (phzR) and non-heme chloroperoxidase (cpo), which play a major role in the synthesis of pyrrolnitrin. Furthermore, a large number of genes associated with detoxification of reactive oxygen species (ROS) and superoxide radicals were observed in the rhizosphere of non-suppressive soils. This would be a response of wheat roots to the infection by R. solani AG8 (Hayden et al. 2018).

24.6

Metatranscriptomics in Plant Growth Promotion

Plant roots are colonised by a group of soil bacteria which promote plant growth either directly by nitrogen fixation, phosphate solubilisation and plant hormone production or indirectly through production of siderophore, ammonia and hydrogen cyanide. These soil bacteria are referred to as plant growth promoting rhizobacteria (PGPR). PGPR have been reported to induce various biochemical changes in plants with respect to their growth and nutrition (Bashan and Holguin 2004). This may be attributed to the complex amalgamations of several PGPR-stimulated machineries that influence both plant growth and nutrition. They include siderophore production for absorption of iron, synthesis and release of plant hormones such as IAA, and solubilisation of phosphates, minerals and nutrients (Mayak et al. 2004; Gamalero et al. 2010; Shariati et al. 2017). They synthesise various secondary metabolites, enzymes and hormones, which aids in the development of plant roots. They also influence the biochemical reactions of roots by shifting the transcription and biosynthesis of metabolite in cells. Furthermore, transcriptomic studies were conducted to elucidate the molecular mechanism variations in plants associated with PGPRfacilitated growth. In order to go further to realise PGPR as an effective device for agricultural crops, the chief mechanisms used by the specified bacteria must be reviewed comprehensively. Plants in their typical habitat are encircled by a huge variety of microbes, of which a few microbes interact with plants directly through mutualism, while others colonise the plant and exhibit commensalism. Furthermore, the plants are influenced by these microbes to alter their environments (Schenk et al. 2012). The microbiomes associated with plants can enhance plant growth or restrict plant pathogens (Arif et al. 2020). Understanding of plant-microbe interactions may effectively give rise to innovative approaches to improve plant productivity (Schenk et al. 2012). Metatranscriptomics helps discover the potentially interesting (yet unknown) plant-microbe relationships. When plants are under multiple biotic and abiotic stresses, they first prioritise their physiological pathway to cope with stress that can determine the outcome of plant-microbe interactions (Yao et al. 2011; Schenk et al. 2012) and microbial community. In contrast, alteration of the microbiome with PGPR consortia can improve plant growth and alleviate the stress caused by biotic and/or abiotic factors. Manipulation of plants by microbiome engineering either by direct or indirect approaches is an emergent strategy to enhance crop yield and

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resilience (Arif et al. 2020). Metatranscriptomics helps in rhizosphere microbiome engineering through categorisation and quantification of functionally expressed microbial genes that benefit a wide variety of crop plants (Arif et al. 2020). Malviya et al. (2019) performed a comparative study on sugarcane root transcriptome to understand their response to Burkholderia anthina (MYSP113). The results revealed the involvement of many genes in response to strain B. anthaina MYSP113 and significantly enriched in terms of quantity. These genes were related to several processes, such as nitrogen metabolism, plant hormone and signal transduction. Furthermore, enzyme actions, such as superoxide dismutase and peroxidase, were substantially enriched in roots after B. anthaina MYSP113 inoculation.

24.7

Metatranscriptomics in Abiotic Stress Tolerance

The impact of abiotic stress on plants and its mitigation through microorganisms have been well documented both at the physiological and molecular levels. Among the various abiotic stresses, water deficit, which has affected about 64% of the total area globally, remains a major stress for plants and causes significant loss in crop growth and yield (Mittler 2006; Cramer et al. 2011). Plant-microbe interactions can be well elucidated with the help of methodologies such as microarray and mRNA sequencing, which can generate information at the transcriptome level (Akpinar et al. 2015; Budak and Akpinar 2015; Wang et al. 2016). A comparison of transcripts in biological systems expressed under two different conditions would help in understanding the role of transcripts in combating the negative effects of stresses on plants. A comparative study of the transcription profiles of two Sinorhizobium meliloti strains (1021 and RD64) revealed that RpoH1, a sigma factor coding gene, and other stress related genes were found to be induced in strain RD64 (this strain overproduces IAA). The induction of stress-related genes was also reported in IAA overproducing Sinorhizobium meliloti by Defez et al. (2016). During a transcriptome analysis of rapeseed inoculated with Stenotrophomonas rhizophila, a novel plant growth regulatory molecule, spermidine was identified by Alavi et al. (2013). MicroRNAs (miRNAs) are single-stranded non-coding RNAs with a nucleotide length of 19–23. Diverse miRNAs are reported to play vital roles in plants such as rice, Arabidopsis and Medicago by regulating various biochemical processes in response to abiotic stresses like drought, salinity and cold (Trindade et al. 2010; Budak and Akpinar 2015). The importance of miRNA in the regulation of tolerance against salinity in Arabiodopsis (miR393), and alleviation of drought and salinity in rice (miR169) through modulation of transcription factor (NF-YA) expression has been reported (Zhao et al. 2009; Gao et al. 2011). In tomato, tolerance to drought was conferred owing to miR169c overexpression, which regulates the expression of gene (s) responsible for stomatal activity (Zhang et al. 2011). In cucumber, stress tolerance is mainly mediated by WD-repeat proteins which are regulated by miRNA, Bvu-miR13 (Li et al. 2014). Besides regulating the transcription factors (TFs), miRNAs also control stress-signalling pathways which are involved in the development of roots and leaves (Curaba et al. 2014). The regulation of superoxide dismutases, SOD1 and SOD2, was mediated by miR398 through the reduction of ROS (Kantar et al. 2011). Various kinds of miRNAs mitigate abiotic stress through

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modulation of diverse cellular reactions and metabolic processes like regulation of transcription, ion transport, apoptosis and auxin homeostasis (Li et al. 2010). They also have been reported for regulation of stress response in plants against aluminium stress. The expression profile of miRNAs in two different subspecies of rice, that is, japonica and indica, which showed different tolerance to aluminium stress, was compared. The results unveiled 16 unique kinds of miRNA responses that revealed an exhibition of complex responses under aluminium stress (Lima et al. 2011). In plants, irreversible damages are being caused by flooding and radiation through generation of ROS (Blokhina and Fagerstedt 2010). In Arabidopsis, the regulation of miR398 and SOD proteins is vital under oxidative stress (Sunkar et al. 2006). In Populus tremula, miR398 induction and miR395 down-regulation were detected during the process of UV-B stress alleviation (Jia et al. 2009). The cold temperature harshly disturbs sugar beet seedlings and recovery of sugar from them after harvest. Transcriptome profiling of leaves and roots from cold-stressed plants unveiled that the CBF3 gene was up-regulated faster in tissues of roots than in leaves (Moliterni et al. 2015). Up-regulation of genes from the AP2/ERF family, which involve in jasmonic-acid-mediated responses, was detected under cold stress (Licausi et al. 2013).

24.8

Challenges

The application of metatranscriptomics may be limited due to the fact that a. predominance of ribosomal RNA significantly reduces the coverage of mRNA, b. the stability of mRNA is very minimum, c. challenges in differentiating the host and microbial RNA despite the availability of enrichments kits (Aguiar-Pulido et al. 2016), and d. the absence of polyA tailed bacterial and archaeal mRNAs which consequently results in reduced recovery of expressed mRNAs after their extraction (Maela and Serepa-Dlamini 2020). Another limitation is that due to the absence of good-quality and assembled reference genomes, the transcripts are seldom assigned to particular microbes (Levy et al. 2018). These challenges have to be taken care of while deciphering the role of rhizosphere metatranscriptomics in plant growth improvement.

24.9

Conclusion

Metatransciptomics plays an imperative role in understanding the dynamics of the rhizosphere microbiome, under various biotic and abiotic stress conditions, to develop a comprehensive catalogue of microbes and their functions in order to develop a blueprint for rhizosphere engineering. It can be concluded from the literature that most of the genes are obtained in dynamic root-associated microorganisms, which is evidenced by the enrichment of gene expression in the root zones as compared to the soil. This is attributed to the production of various

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metabolites and substances that support the growth and development of rhizosphere microflora, which in return helps mitigate the biotic and abiotic stresses (Table 24.2).

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Rhizospheric Engineering for Sustainable Production of Horticultural Crops

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Sarita Devi and Poonam Kumari

Abstract

Rhizosphere- and root-associated bacteria are vital components of plant microbiomes and affect the physiology and development of plants. For sustainable production of horticultural crops, it is essential to know about the diversity of the microbes associated with such crops and how the soil factors affect the microbiome. To improve the health and productivity of horticultural crops, various techniques for manipulating plants and their root-associated microorganisms have been studied so far. Some approaches are focused on understanding interactions between roots, microbes and soil, while others are focused on plant mechanisms that affect development. Plants, for example, can be modified to change the rhizosphere’s pH or release substances that boost food availability, defend against biotic and abiotic stresses, or promote the production of beneficial microbes. Novel molecular techniques and significant biotechnological advancements will help gain a better understanding of the complex chemical and biological interactions that occur in the rhizosphere, ensuring that rhizosphere engineering approaches are both safe and helpful in enhancing the productivity and quality of horticultural crops. This chapter provides an insight into various rhizospheric microbes associated with horticultural crops and their manipulation for sustainable crop production.

S. Devi Division of Biotechnology, CSIR-Institute of Himalayan Bioresource Technology, Palampur, Himachal Pradesh, India P. Kumari (*) Division of Agrotechnology, CSIR-Institute of Himalayan Bioresource Technology, Palampur, Himachal Pradesh, India e-mail: [email protected] # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2022 U. B. Singh et al. (eds.), Re-visiting the Rhizosphere Eco-system for Agricultural Sustainability, Rhizosphere Biology, https://doi.org/10.1007/978-981-19-4101-6_25

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Introduction

Life on the earth is sustained with the aid of a small soil volume surrounding the roots, known as the rhizosphere. The soil is where much of our planet’s biodiversity occurs, and perhaps the most diverse environment on Earth is provided by the rhizosphere; and it is definitely considered the most significant zone in terms of determining the quantity and quality of human food resource (Hinsinger et al. 2009). Very little information about the functioning of the rhizosphere is available, considering its central significance to all forms of life, and we have an incredible ignorance about how best we can use it to our benefit (Almalak 2018). The rhizosphere acts as a hot spot for various microbial interactions as the plant roots’ exudates provide a major food source for microorganisms and an impetus of their populace density and related activities (Hinsinger et al. 2009). There are many rhizospheric microbes with an impartial effect on the plant, but it often attracts microorganisms that have useful or harmful effects on the plant (Mendes et al. 2013). Pathogenic fungi, oomycetes, bacteria and nematodes are the microorganisms which adversely affect plant growth and health (Mendes et al. 2013). Most of the soil inhabitant pathogenic microorganisms are developed in the bulk soil to prosper and grow, but the rhizosphere is the playground and contagion court where the pathogenic microorganisms develop a parasitic relationship with the plant (Fageria 2012; Qu et al. 2020). The rhizosphere is also a battleground where microfauna, microflora and the complex rhizosphere community act together with pathogens and affect the consequence of pathogen infection (Hinsinger et al. 2009). The plant benefits from a wide variety of microorganisms, including nitrogen-fixing bacteria, ecto- and endomycorrhizal fungi, plant growth-promoting bacteria and fungi (McNear Jr 2013). In comparison to synthetic fertilisers, pesticides and insecticides, plant growth-promoting rhizobacteria are known to improve plant performance through various mechanisms, such as production of advantageous hormones, improvement in plant nutritional status and decrease in stress-related damage (Bhattacharyya and Jha 2012; Gouda et al. 2018). The association between plants and plant growth-promoting rhizobacteria (PGPR) is of particular interest as they enhance growth and development of crops in various stress conditions such as high or low temperatures, soil salinity, nutrient deficiency and drought (Schillaci et al. 2019). There are various forms of plant growth-promoting rhizobacteria populations present in the rhizospheric soil, which show beneficial effects on the production of crop. Numerous investigations are done to understand the dynamics diversity and importance of soil plant growth-promoting rhizobacterial communities and their cooperative and beneficial roles in the productivity of various crops (Gupta et al. 2015; Aloo et al. 2019). The most common examples of plant growth-promoting rhizobacterial genera showing plant growth-promoting activity include Erwinia, Azotobacter, Pseudomonas, Mesorhizobium, Azospirillum, Bacillus, Enterobacter, Burkholdaria, Mycobacterium, Rhizobium and Flavobacterium (Ahemad and Kibret 2014). In the era of globalisation and modernisation, crop sustainability is a challenge. Agricultural systems and activities aimed at conserving or enriching the health of natural resources are related to sustainable farming. Certainly, horticultural practices

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have some impact on the natural resources used to grow fruits, vegetables, flowers and other products. Horticultural industries are becoming increasingly concerned with preserving and protecting their resource base and environment as the understanding of sustainability problems increases. With the world population growing at an unprecedented pace, crop production needs to be increased in order to meet global food requirements and, at the same time, boost agricultural sustainability. Feeding the human population, which is estimated to rise from 7.6 billion now to 9.5–10 billion by 2050, will be a huge challenge for scientists around the world. In recent times, crop production is facing severe threats because of numerous abiotic and biotic stresses, as well as reduced land supply. In nature, plants are exposed to trillions of microbes that colonise and occupy different plant chambers or compartments such as the rhizosphere, the rhizoplane, the endosphere and the phyllosphere, therefore considered a secondary plant genome (Kumar and Dubey 2020). The rhizosphere has a large pool of soil microbes and is considered the ‘hot spot’ for microbial colonisation and activity. It is known as the world’s largest ecosystem with tremendous energy flux (Barriuso et al. 2008). The rhizospheric microflora protects against diseases, improves growth by producing phytohormones and can enable plants to withstand environmental disruptions such as irregular changes in temperature, drought and salinity. Knowing the importance of the rhizosphere and its manipulation in sustainable crop production, this chapter aims to discuss the role of the rhizosphere and rhizospheric engineering in horticultural crops.

25.2

Rhizosphere

The soil is the world’s most important biodiversity reservoir, and it serves as a vital habitat for prokaryotes and a wide spectrum of eukaryotes, including fungi among other soil microorganisms and a diverse range of invertebrates. The diversity of soil prokaryotes is predicted to be three orders of magnitude larger than the diversity of prokaryotes found in all other ecosystems or ecological sections on the world (Curtis et al. 2002; Hinsinger et al. 2009). Higher plant roots anchor the terrestrial habitats’ above-ground diversity, and make available most of the carbon to power the soil environment. The soil is much more significant from a functional viewpoint, in addition to their role in biodiversity, in maintaining all other aspects of terrestrial biodiversity and providing many ecological unit services (Bach et al. 2020). The temporal and spatial heterogeneities from nanometre to kilometre scales are a significant characteristic of soils (Bach et al. 2020). The environmental heterogeneity and spatial distance’s interactions are important factors influencing the abundance and relatedness of the Burkholderia cepacia rhizosphere-bacteria complex (Ramette and Tiedje 2007). In addition to species diversity, abundances of species are also significant in soils (Watt et al. 2006). Approximately 104 nematodes, 104 protozoa, 107–1012 bacteria and 5–25 km of fungal hyphae are present in 1 g of soil, with an average specific surface area of about 20 m2 g 1 and the very small size of most of these microorganisms, their

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Table 25.1 Composition of root exudates S. no. 1

Compositions Amino acid and amide

2 3

Enzyme Growth factor

4 5

Phenolic acid and coumarin Sugar

6

Organic acid

7

Others

Elements identified Serine/homoserine, proline, phenylalanine, methionine, lysine, histidine, glycine, glutamine, cystine/cysteine, aspartic acid, asparagine, arginine and alanine Polygalacturonase, protease, phosphatase, invertase and amylase Thiamine, pyridoxine, p-amino benzoic acid, pantothenate, niacin, n-methyl nicotinic acid, inositol, choline, biotin and auxins Vanillic acid, syringic acid, salicylic acid, ferulic acid, cinnamic acid, coumarin and caffeic acid Xylose, sucrose, ribose, rhamnose, raffinose, oligosaccharide, maltose, glucose, galactose, fucose, fructose and arabinose Valeric, tartaric, succinic, pyruvic, propionic, oxalic, malonic, malic, maleic, lactic, glutaric, citric, butyric and acetic acid Sterols, proteins, lipids, nucleotides, flavanone, fatty acids, carbohydrates, aromatics and aliphatics

surface coverage amounts in total to only 10 5 to 10 6% of the total soil surface area (Hinsinger et al. 2009). The soil can be compared to a vast desert, where life is dispersed discreetly, especially when the tendency of many of these bacteria in soil to form colonies and gather, resulting in activity hotspots, is taken into account (Pointing and Belnap 2012; Makhalanyane et al. 2015). One of the most fascinating hotspots of activity and diversity in soils is the rhizosphere (Jones and Hinsinger 2008). The rhizosphere is well-described as the soil amount around living roots, which is affected by root activity (the ‘Einflusssphäre der Wurzel’) according to Hiltner 1904 in Hartmann et al. (2008). To define the soil area under the control of plant roots, Hiltner coined the word ‘rhizosphere’ in 1904. Our cognizance of the subject has significantly improved over time. The rhizosphere is now better described as the ‘field of action or effect of a root’. The rhizosphere is considered a limited area of soil under the influence of live roots, where root exudates can encourage or constrain microbial communities and their activities (details of the same are given in Table 25.1, Pinton et al. 2007; Backer et al. 2018). Because of the release of root exudates that stimulate or inhibit rhizosphere organisms, the rhizospheric zone is characterised by intense biological activity. The dynamics and complexity of this area are further characterised by the interactions between the soil, the plants and the organisms that form the rhizosphere (Pinton et al. 2007). For several bacterial and fungal species, the root surface or rhizoplane also provides a highly favourable nutrient base, and these two zones together are sometimes denoted as the soil-plant interface (Nihorimbere et al. 2011). Although the rhizosphere is an incessant zone, it is useful to define the endorhizosphere as the root’s cell layers and the ectorhizosphere as the area around the root. As a result, the rhizosphere is a component of the soil environment in which the plant roots, the soil, and the soil bacteria (biota) interact. In the rhizosphere, plant/microbe and plant/faunal interactions also abound (Pinton et al. 2007). These interactions vary from symbiotic relationships (e.g. mycorrhizal associations and nitrogen fixation) to pathogenic

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interactions. When the rhizosphere ecology is considered, management strategies such as biological control and bioremediation can also be effective (Igiehon and Babalola 2018). A better understanding of the rhizosphere and its impact on different organisms that occupy this region would allow manipulations of the environs that support the production of plants and the environs.

25.3

Rhizospheric Microbes and Their Interactions with Plants

Numerous investigations have shown that soil-borne microbes interact at the rootsoil interface with plant roots and soil constituents. The wide range of root-microbe interactions contributes to the dynamic rhizospheric ecosystem development in which microbial communities interact as well (Barea et al. 2005). When compared to root-free bulk soil, the chemical, physical and biological features of the soil associated with roots are responsible for vicissitudes in various microbial communities as well as growing numbers and activity of microorganisms in the micro-environment of the rhizosphere (Barea et al. 2005; Jacoby et al. 2017). The essential determinants of the functions of the rhizosphere are the carbon fluxes (Toal et al. 2000). For the heterotrophic soil biota, the release of decaying plant material and root exudates as structural material, growth substrates or signals for the microbiomes associated with root provides sources of carbon compounds (Canarini et al. 2019). Microbial activity in the rhizosphere regulates rooting patterns and the delivery of accessible nutrients to plants by modifying the quantity and quality of root exudates in the process (Barea et al. 2005). Furthermore, in the rhizosphere, two kinds of interactions are identified: interactions based on detritus (dead plant material) that affect nutrient and energy flows, and interactions based on living plant roots. Both types of interactions can be used in ecology and agronomy (Barea et al. 2005). In addition, the rhizosphere is made up of three distinct yet interconnected elements: the rhizoplane, the rhizosphere (soil) and the root itself. Including the firmly adhering soil particles, the rhizoplane is the root surface, while the rhizosphere is the region of the soil impacted by roots by the release of substrates that affect microbial activity. The root, the aforementioned, is part of the rhizosphere system, as some microbes (e.g. the endophytes) are able to colonise root tissues (Rizvi et al. 2009; Nihorimbere et al. 2011). Root colonisation is the microbial colonisation of the rhizoplane and/or root tissue, whereas rhizosphere colonisation is the colonisation of the nearby soil volume, under the effect of the root (Barea et al. 2005; Rizvi et al. 2009). The use of molecular techniques to categorise various microbes is a crucial tool for understanding the ecology of the rhizosphere (Pühler et al. 2004). Because of current public uncertainties about the negative effects of agro-chemicals, there is a growing interest in better understanding the cooperative interactions within rhizosphere microbial communities and how these could be advantageous to diverse crop production (Barea et al. 2005). Some cooperative microbial activities could be used as low-input biotechnology methods, forming the foundation of a technique to promote environmentally benign, sustainable

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practices that are critical for the productivity and stability of both natural and agricultural ecosystems (Arora et al. 2010). In the rhizosphere, microbial communities and other agents include bacteria, fungi, nematodes, algae, protozoa and microarthropods (Barea et al. 2005). Many members of this rhizospheric group have very little or neutral effect on the plant, but they are important elements of the intricate food web that consumes the massive amounts of carbon that the plant fixes and releases into the rhizosphere (i.e. rhizodeposits). The microbial population present in the rhizosphere often includes members that possess beneficial or deleterious effects on the plant. The pathogenic fungi, oomycetes, bacteria and nematodes adversely affect plant growth and health, while microorganisms that are beneficial include nitrogen-fixation, mycorrhizal interactions, promotion and inhibition of plant growth. Also, biological regulation and bioremediation have been investigated in recent years. Nitrogen-fixing bacteria may make nitrogen available to the plant that is not available otherwise. The nodules on the roots of plants are produced from Rhizobia and associated bacteria (Lindström and Mousavi 2019). As the plant provides protection and nutrients for the bacteria and the bacteria provide nitrogen to the plant, they share mutually beneficial relationship. The associations with plants are also created by other nitrogen-fixing species. This can also include other plant growth-promoting compounds along with plant-available nitrogen (Lindström and Mousavi 2019). Until now, taxonomists have recognised numerous species in the genus Azospirillum, viz. A. amazonense, A. halopraeferens, A. lipoferum, A. irakense and A. brasilense (Srivastava et al. 2015), A. picis (Lin et al. 2009), A. canadense (Mehnaz et al. 2007a), A. melinis (Peng et al. 2006), A. zeae (Mehnaz et al. 2007b), A. doebereinrae (Eckert et al. 2001) and A. rugosum (Young et al. 2008). Azospirillum is known to have more effective nitrogenase properties than other nitrogen fixers, among the free-living nitrogen-fixing bacteria. Azospirilluminoculated plants have been demonstrated to absorb solution nutrients faster than uninoculated plants, resulting in higher levels of dry matter, phosphorus, nitrogen and potassium in the leaf foliage (Srivastava et al. 2015). In addition to being one of the indices of soil quality, soil microbial diversity varies on a regular basis in response to management techniques. The effects of 12 years of traditional and sustainable management practices on the metabolic diversity and soil microbial composition of a mature rainfed olive orchard revealed that soil under sustainable practices had more culturable fungi, bacteria, soil enzyme activity and microbial population metabolic diversity indices than that under traditional practices (Sofo et al. 2014). These alterations in soil microbial communities have reacted favourably to improvements in olive fruit production and quality (Sofo et al. 2010). Sofo et al. (2010) observed greater magnitude of quantitative and qualitative vicissitudes in soil microbial communities in kiwi and peach fruit orchards in response to innovative (characterised by minimal tillage, organic matter inputs from composts and cover crops, water, pruning, and adequate irrigation and fertilisation) than in traditional soil management systems (characterised by conventional tillage, zero organic input, empirical pruning, excessive irrigation and strong chemical fertilisation). A great number of microorganisms have shown their usefulness in a variety of fruit crops,

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both as pure culture (as broth) and as carrier-based cultures (Table 25.2). These results provide strong support for the need to fine-tune such efficient microorganisms in combination with inorganic fertilisers and organic manures so that their multidimensional value-added response is seen in perennial fruit crops (Srivastava et al. 2015). The mycorrhizal fungi, without causing root disease, often create a mutualistic symbiosis with plants and infect roots. In the rhizosphere of most plants, these fungi can be found and form associations with all gymnosperms and more than 79 percent of monocotyledonous and 83 percent of dichotyledonous plants. On the outside (ectomychorrhizae) or inside (endomycorrhizae) of plant roots, the mycorrhizal fungi may also form structures (Warburton et al. 2005). The fungal hyphae cause a greater volume of soil to be contacted by the roots. The solubilisation of nutrients (e.g. phosphorus) is increased by certain types of mycorrhizal fungi. They help the plants/crops increase selective ion uptake and nutrient absorption mainly in stressed environments (e.g. soils with phosphorus and water deficiency), and protect them from environmental extremes (Warburton et al. 2005; Begum et al. 2019). Plant exudation patterns can be modified by these fungi after colonisation, thereby affecting the macrofaunal and microbial populations of the rhizosphere (Bais et al. 2006). Fungi can also shield plant roots from pathogens’ invasion. Endomycorrhizal extra radicle hyphae secrete glomalin, a glycoprotein that aggregates soil particles, strengthens water-stable aggregates and enhances the structure of the soil (Warburton et al. 2005). This association may improve plant growth and survival, particularly in low-nutrient or adverse environments, and may have a potential for disturbed sites to re-vegetate. The abundance and diversity of beneficial and harmful bacteria are related to the quantity and kind of rhizodeposits, as well as to the consequences of microbial interactions that occur in the rhizosphere (Somers et al. 2004). It has piqued the interest of scientists from several disciplines who want to learn more about the processes that determine the structure, behaviour and dynamics of the rhizospheric microflora, and how they might be used to develop innovative plant growth and health strategies.

25.4

Plant Growth-Promoting Rhizobacteria

Plant growth-promoting rhizobacteria are basically beneficial microorganisms present in the soil. For such microorganisms, the expression ‘plant growth promoting rhizobacteria’ is used because they either directly contribute to the growth activities of plants or indirectly enhance plant growth and development (Lugtenberg and Kamilova 2009; Siyar et al. 2019). There are numerous plant growth-promoting rhizobacterial species that improve plant growth and overall efficiency. Plant growth-promoting rhizobacteria may be free-living (different species of Pseudomonas, Agrobacterium, Bacillus, Burkholderia etc.) or may be in symbiotic associations with their hosts (various species of Rhizobium, Frankia etc., Podile and Kishore 2006; Bhattacharyya and Jha 2012; Siyar et al. 2019). To stimulate the growth of plants through a variety of ways, both free-living and endophytic species

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Table 25.2 Response of various rhizospheric microbes on yield, nutrient uptake and growth of fruit crops S. no. 1.

2.

3.

4.

5.

6.

7.

8.

9.

10.

11.

12.

Fruit crop Malus domestica Borkh. (Apple) Malus domestica Borkh. (Apple) Malus domestica Borkh. (Apple) Prunus armeniaca L. (Apricot) Prunus armeniaca L. (Apricot) Musa acuminata L. (Banana) Musa acuminata L. (Banana) Musa acuminata L. (Banana) Mangifera indica L. (Mango) Passiflora edulis Sims. (Passion fruit) Citrus sinensis Osbeck (Sweet orange) Vitis vinifera L. (Grape)

Response parameters Yield, growth and plant nutrition

Microbes involved Microbacterium, Bacillus (M3), Bacillus (OSU-143)

Reference Karlidag et al. (2007)

Fruit yield and tree growth

Pseudomonas(BA-8), Bacillus(OSU 142, M-3)

Aslantaş et al. (2007)

Root growth, germination and pest incidence

Trichoderma viride, Pseudomonas striata, Azotobacter chroococcum-

Raman (2012)

Leaf nutrient concentration, shoot length and yield Yield, growth and leaf nutrient composition

Bacillus (OSU-142)

Esitken et al. (2006) Pirlak et al. (2007) Jeeva et al. (1988)

Leaf area and yield, girth and height and of pseudo-mostem Leaf area, bunch weight and number of fingers Fruit weight and finger size

Pseudomonas(BA-8), Bacillus (OSU-142) Azospirillium sp.

Azospirillum brasilense, Azotobacter chroococcum Pseudomonas fluorescens, Azospirillum brasilense

Number of leaves and seedling diameter

Azotobacter chroococcum

Improved plantlet growth and yield Growth, fruit yield and nutrient uptake

Trichoderma sp., Azospirillum sp., Azotobacter sp. Glomus fasiculatum, Azospirillum brasilense

Root development

Pseudomonas fluorescens

13.

Pyrus pashia (Quince)

Yield and fruit properties

Bacillus T8 and Bacillus OSU-142

14.

Punica granatum (Pomegranate)

Vigorous plant growth and thrive under stressed soils

N2-fixing bacteria or AM fungi

Tiwary and Hasan (1999) Suresh and Hasan (2001) Kerni and Gupta (1986) QuirogaRojas et al. (2012) Singh and Sharma (1993) Wange and Ranawade (1998) Arıkan et al. (2013) Aseri et al. (2008) (continued)

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Table 25.2 (continued) S. no. 15.

Fruit crop Juglans regia (Walnut)

Response parameters Plant height, dry weight, P and N uptake of seedlings

Microbes involved Pseudomonas chlororaphis and Pseudomonas fluorescens

Reference Yu et al. (2011)

of plant growth-promoting rhizobacteria have been identified. They can yield various types of organic compounds that can be involved in direct plant-growth promotion (Pérez-Montaño et al. 2014). Some plant growth-promoting rhizobacteria are known to solubilise and make available phosphate and iron to plants (Ahemad and Iqbal 2017; Alori et al. 2017; Siyar et al. 2019). Indirectly, by disrupting a broad range of plant pathogens and disease severity, plant growth-promoting rhizobacteria can stimulate the growth potential of host plants (Xiang et al. 2017; Liu et al. 2017). As crops, similar to their wild counterparts, are equally threatened by various stresses, understanding and elucidating the influences of plant growth-promoting rhizobacteria on their growth and development will contribute to the sustainability of crop production.

25.4.1 Types and Underlying Mechanisms of Plant Growth-Promoting Rhizobacteria Plant growth-promoting rhizobacteria are of different kinds and origin. The microorganisms are copiously present as free-living in the rhizosphere where they do not form any symbiotic association with other species. The species of Azospirillum, Arthrobacter, Erwinia, Flavobacterium, Pseudomonas, Agrobacterium, Serratia, Micrococcous, Azotobacter, Caulobacter, Burkholderia, Bacillus and many others are well-known examples of free-living plant growthpromoting rhizobacteria, while those of symbiotic plant growth-promoting rhizobacteria are Azorhizobium, Allorhizobium, Mesorhizobium, Bradyrhizobium, Rhizobium, Frankia and so on (Compant et al. 2010; Bhattacharyya and Jha 2012). The dissemination of symbiotic and free-living plant growth-promoting rhizobacteria is ecologically regulated in the rhizosphere, depending on several aspects such as the availability of soil nutrients, the rhizosphere’s water status and vegetation type. The root exudates produced by plants are one of the leading drivers of rhizobacterial dynamic modulation (Siyar et al. 2019). Citric acids produced by cucumber roots have been effective in the root colonisation of the host plants with plant growth-promoting rhizobacteria (Zhang et al. 2014). The role of secondary metabolites released from the host roots in the effective interaction between plant growth-promoting rhizobacteria and plants was described by Huang et al. (2014). Ahemad and Kibret (2014) suggested that amino acids, organic acids, carbohydrates, vitamins, enzymes and various inorganic salts are found in the root zone, which can drive plant growth-promoting rhizobacteria to the root surfaces or the rhizosphere in a particular zone. Rasmann and Turlings

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Fig. 25.1 An illustration of the mechanism of action of PGPR in plant growth improvement

(2016) indicated that roots produced organic compounds that serve as ‘attracting’ signals for plant growth-promoting rhizobacteria accommodation in the root region. Schulz-Bohm et al. (2018) indicated that various volatile organic compounds produced by the plant roots play a significant part in attracting plant growth-promoting rhizobacteria and the symbiotic association formation. Figure 25.1 provides an example of the mode of action of plant growth-promoting rhizobacteria in promoting plant growth. The stimulation of plant growth by plant growth-promoting rhizobacteria occurs primarily through two mechanisms that is, primary and indirect mechanisms. Direct growth promotion is assisted by plant growth-promoting rhizobacteria when they produce several types of organic molecules which range from enzymes, amino acids and carbohydrates to inorganic substances (Ahemad and Kibret 2014). Certain plant growth-promoting rhizobacteria species can directly boost growth and development of plants by producing hormones and growthregulating substances such as abscisic acid, auxins, gibberellic acid and cytokinins, (Timmusk et al. 2017). Several free-living species similar to those associated with legumenous plants can fix nitrogen and thus help plants meet their nitrogen requirement (Pham et al. 2017; Siyar et al. 2019). Chauhan et al. (2017) presented evidence that Aneurinibacillus aneurinilyticus strains were able to efficiently convert phosphate to soluble forms and nitrogen to simple forms. The Pseudomonas, Erwinia, Flavobacterium, Aerobacter and Bacillus species have also been reported for phosphate solubilisation and growth improvement of various plants (Hayat et al. 2010). The active role played by plant growth-promoting rhizobacteria in reducing salinity stress (Shrivastava and Kumar 2015; Kumar et al. 2018; Siyar et al. 2019), drought

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tolerance (Jatan et al. 2019), remediation of heavy metals (Sobariu et al. 2017; Saif and Khan 2017) and disease resistance and disease intensity reduction are indirect mechanisms involved in plant-growth enhancement (Verma et al. 2018). Majeed et al. (2018) suggested that there are several plant growth-promoting rhizobacterial strains that induce systemic plant resistance to various pathogens and suppress pathogenic agents directly through antagonism, competition and antipathogenic compounds.

25.5

Effects of Plant Growth Promoting Rhizobacteria

The plant growth-promoting rhizobacteria influence plants, both indirectly and directly. These rhizobacteria directly supply substances synthesised by bacteria or promote the absorption of certain plant nutrients from the atmosphere to the plant. The plant growth-promoting rhizobacteria counteract the negative effects of one or more phytopathogenic microbes, resulting in indirect plant-growth promotion (Kokalis et al. 2002; Ortega et al. 2017).

25.5.1 Biological Nitrogen Fixation The nitrogen-fixing microbes can live in symbiosis or freely with some plants, specifically with legumes where they produce root nodules. These microorganisms take nitrogen from the air and provide it to plants in the form of assimilable compounds, collecting carbohydrates from the roots in the process (Ortega et al. 2017). Some examples of vegetable inoculation with nitrogen-fixing PGPR are Rhizobium sp. TN42, Azotobacter chroococcum in potato (Naqqash et al. 2016), Azotobacter + PSB in radish (Ziaf et al. 2016), Azotobacter, Azospirillum and VAM in cabbage (Sharma et al. 2013).

25.5.2 Solubilisation of Phosphorus Phosphorus is one of the significant macronutrients in plants, along with nitrogen and potassium. Although agricultural soil normally has adequate amounts of phosphorus due to fertiliser inputs, most of it is generally not accessible to plants in insoluble form. However, there are several microbes which are able to convert insoluble phosphorus to orthophosphates, a soluble form (Chen et al. 2006; Selvakumar et al. 2009). Many microbes are identified in the rhizosphere of horticultural crops with phosphate solubilisation effects such as Bacillus megaterium TV-91C, Pantoea agglomerans RK-92 and B. subtilis TV-17C in cabbage (Turan et al. 2014), Agrobacterium rubi A16, Burkholderia gladii BA7, P. putida BA8, B. subtilis OSU142, B. megaterium M3 in mint (Kaymak et al. 2008), Azospirillum, Pseudomonas fluorescens, and Bacillus subtilis in bitter gourd (Kumar et al. 2012).

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25.5.3 Production of Stimulants of Plant Growth Phytohormones such as cytokinins, gibberellins, auxins and ethylene are released by plant growth-promoting rhizobacteria, which influence a variety of activities like stem and root growth, flowering and fruit production (Ahmad et al. 2005; Ortega et al. 2017).

25.5.4 Antagonistic Activity and Biocontrol Agents The bacteria that reduce plant disease incidence are regarded as biocontrol agents (Beattie 2007), whereas antagonists are the microbes that have antagonistic behaviour against plant pathogens (Ortega et al. 2017). Among these activities, the following actions can be illustrated. (a) Hydrolytic enzyme synthesis: The different hydrolytic enzymes, for example, proteases, glucanases, chitinases and lipases, are synthesised that can lyse pathogenic fungal cells (Maksimov et al. 2011). (b) Siderophores production: In iron (Fe)-limiting situations, plant growthpromoting rhizobacteria can create siderophores, which are iron-chelating chemicals that trap the available iron and deliver it to plants, encouraging their growth (Whipps 2001). It also has an antagonistic influence by stopping iron from being taken from the soil by other harmful bacteria and fungi. Four kinds of bacterial siderophores are classified as hydroxamates, carboxylates, phenol catecholates and pyoverdines (Crowley 2006). (c) Antibiotics production: There are six groups of antibiotic compounds produced by plant growth-promoting rhizobacteria that are associated with root disease control, according to Haas and Défago (2005), which include phloroglucinols, phenazines, pyrrolnitrin, pyoluteorin, hydrogen cyanide and cyclic lipopeptides. In addition to other antibiotics, the pathogenic bacteria and fungi are active against colistin polymyxin and circulin (Ortega et al. 2017).

25.5.5 Induced Systemic Resistance and Systemic Acquired Resistance Induced systemic resistance and acquired systemic resistance are two distinct events in plants, yet both trigger an immunological response to pathogenic agents. Induced systemic resistance consists of plant growth-promoting rhizobacteria or non-pathogenic rhizobacteria-induced self-plant resistance (Pieterse et al. 2003). Systemic acquired resistance is resistance that develops as a result of exposure to a pathogen. Induced systemic resistance and systemic acquired resistance act via different metabolic pathways. Although systemic acquired resistance induction is done via salicylic acid, jasmonic acid is required for induced systemic resistance (Pieterse et al. 2003). Induced systemic resistance-mediated protection is

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considerably lower than that provided by systemic acquired resistance (Van Loon 2000). Nevertheless, the two forms of protection occur with a greater impact at the same time than each separately (Ortega et al. 2017).

25.5.6 Industrial Applications of Plant Growth-Promoting Rhizobacteria As can be inferred from the above, there are various applications of plant growthpromoting rhizobacteria and typically result in an option that is more environment friendly than pesticides and chemical fertilisers (Vessey 2003; Adesemoye et al. 2009). Optimal plant growth-promoting rhizobacteria for commercialisation must have the ability to contend with other microbes, expedite plant growth, have a large spectrum of activity, and be resistant to UV radiation, heat and oxidising chemicals (Nakkeeran et al. 2005). Despite several decades of commercial application of the Enterobacter, Bacillus, Azotobacter, Klebsiella, Variovorax, Serratia and Azosprillum species and with promising new laboratory studies, their effects on crops are not fully satisfactory (Ortega et al. 2017). For example, the use of plant growth-promoting rhizobacteria as fertiliser includes losses as a result of ecological conditions and runoff, during aerial application. There are, however, numerous ways to help the development of plant growth-promoting rhizobacteria. They are also applied to plant seeds (Bloemberg and Lugtenberg 2001) and, by taking advantage of plant exudates, plant growth-promoting rhizobacteria should be capable of settling in the rhizosphere once sown. Nano encapsulation-based technology, on the other hand, can be used as a tool for the safety of plant growth-promoting rhizobacteria and allow the more regulated release of plant growth-promoting rhizobacteria (Vejan et al. 2016). Experiments with genetic modifications can also enhance the establishment and functionality of the plant growth-promoting rhizobacteria (Ortega et al. 2017). Despite the large number of investigations related to mechanisms adopted by plant growth-promoting rhizobacteria and the mode of their activity, the complexity of interactions between plant growth-promoting rhizobacteria and plants makes it important to broaden the knowledge of this subject. Genetic and molecular research (Bloemberg and Lugtenberg 2001) could make it possible for these interactions in the rhizosphere to understood these better and help create new commercial products. Finally, due to recent developments in bioinformatics, DNA amplification refinement and computational progress, these studies can be reinforced by metagenomic advance (Leveau 2007). This will promote the identification of bacterial species in experimental crops and the tracking of population time periods during culture cycles (Bashan and de-Bashan 2002).

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Rhizosphere Engineering

According to Hiltner (1904), the rhizosphere has been described as the soil compartment that is influenced by plant growth. This effect results from the release of organic materials by the plant, a process called rhizodeposition, consisting mainly of metabolites of plants (exudates) and plant debris (Hartmann et al. 2009). Jones et al. (2009) stated that this carbon loss is a large part of the photosynthetically fixed carbon allocated to the underground root system (from 20 percent to 40 percent). As a result, while most of the bare soils are considered oligotrophic environments, rhizosphere soils are defined as mesotrophic, promoting the growth of bacteria, archaea, viruses and fungal populations (Philippot et al. 2013). These microbes have various effects on the plant and on the overall functioning of the rhizosphere. They are the parts of the carbon cycle that help in the growth and development of plants and also provide resistance against pathogens. Plant rhizodeposition may change qualitatively and quantitatively due to microbial activity affecting microbial components, which is known as the characteristic feedback loop of the rhizosphere that keeps the rhizosphere in a dynamic equilibrium. Such a complex relationship indicates that the rhizosphere can be engineered to promote plant growth and health, or to minimise the effects of different biotic or abiotic stresses, a feature of significant interest in the current global climate change scenario and the need for more sustainable agricultural practices. Basically, all three components of the rhizosphere can be manipulated. The soil can be altered to change its physicochemical properties or improve its overall quality, the plant can be engineered to select or introduce a novel trait of interest, and the microbial populations can be selected to promote plant growth and health. For the development of sustainable agriculture, rhizosphere engineering can improve plant health and change the activity of root-associated bacteria. Rhizobia, Pseudomonas, Bacillus, Burkholderia, Azospirillum, Klebsiella and Gluconacetobacter are among the phytomicrobiomes used in diverse horticultural applications (Rahi 2017). It is important to identify the various root exudate molecules and their interactions with the rhizosphere microflora in order to use the capacity of the rhizosphere for plant growth and the associated climate. Knowing the interactions of the rhizosphere is important for the production of sustainable agroecosystems (Bhatt et al. 2020). Manipulation of the plant and its associated microbes affects the rhizosphere by releasing root exudation molecules that favourably influence microbial signalling compounds. Exudates from the roots differ depending on the genotype and species of the plant. Phytohormones, extracellular enzymes, organic acids, antibiotics, volatile signals and quorum sensing molecules are among the signalling substances secreted by microorganisms (Li et al. 2019). The alteration of plant and rhizosphere microflora for the enrichment of the rhizosphere zone for sustainable agriculture has been investigated in several studies (Fig. 25.2). Plant scientists have created genetically altered plants to address a variety of biotic and abiotic stress problems in the soil. Engineered plants change the pH of the rhizosphere and the secretion of root exudation. This change in the rhizosphere promotes a positive shift in microbial behaviour. Microbial engineering, in addition to plant engineering, is critical in agricultural research, particularly in the

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Fig. 25.2 Rhizosphere engineering for improving plant growth-promoting activities and balancing the soil environment

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areas of PGPR, biological nitrogen fixation, phosphate and iron solubilisation, phytohormone regulation and biocontrol activities (Jochum et al. 2019). Because of the rhizosphere’s numerous interconnected biomes, a shift in these interactions has the potential to alter plant growth and health, and soil qualities. Rhizosphere engineering is promising for soil enhancement, crop quality and production. The engineering of rhizospheres has been supported by a number of research studies. Resistance to major diseases including Pseudomonas syringae and the Xanthomonas genus has been produced using traditional breeding methods. PGPR microbe engineering involves rescuing chromosomes from resistant to susceptible wheat lines, such as replacing the susceptible wheat line S-615 chromosome for Apex chromosome 5B, resulting in SA5B chromosome substituent lines that are as resistant to common rot as Apex (Zhang et al. 2018; Guichard et al. 2019; Chu et al. 2020). Plant density plays a crucial role in phytomicrobiome existence. Traditional breeding considered plant density as an important factor in crop improvement. The genetic capacity for yield and other traits are completely expressed when plants are grown at extremely low plant densities, but it is greatly inhibited at high plant densities (Fasoula 2013). The intimacy of this contact between the plants and their environment is critical for the acquisition of water and nutrients, as well as for beneficial interactions with soil-borne microbes. This same intimacy, however, increases plants’ susceptibility to a variety of biotic and abiotic stresses. Plants have developed a number of mechanisms to adjust the rhizosphere in order to reduce the effects of various environmental stresses, and an understanding of the processes involved can reveal ways in which the rhizosphere can be exploited to improve plant health and productivity. Rhizosphere engineering will eventually minimise our reliance on agrochemicals by replacing their role with helpful bacteria, biodegradable biostimulants or transgenic plants. Some of these materials and procedures are still in the development stage, while others are being tried in the field. Engineered horticulture plants for rhizosphere enrichment are shown in Table 25.3.

25.7

Benefits of Rhizosphere Engineering

Various benefits of rhizosphere engineering in horticultural crops have been illustrated in Fig. 25.3 and discussed below.

25.7.1 Drought Resistance In the twenty-first century, a major problem for agriculture is making the most productive use of water supplies possible. The broad availability of input services such as fertiliser and water has been the basis of modern agricultural production, but it is now widely acknowledged that water shortages are one of the main constraints in meeting the inevitably rising demand for food in the world as the world’s population continues to grow. Therefore, increasing the resistance of plant drought

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Table 25.3 Rhizosphere engineering: engineered horticultural plants for rhizosphere enrichment Engineered Plant/ microbes Papaya Cucumber, Canola

Potato

Lotus corniulatus Citrus sweet orange Radish

Yellow lupin Tomato

Gene Papaya ring spot coat protein gene Pseudomonas fluorescens (CHA 0) transformed with ACC deaminase gene acdS from P. putida UW4 Bacterial lactonase gene Aii A

Host Papaya

Opines biosynthesis gene Pattern recognition receptor FLS 2

Agrobacterium tumefaciens Tobacco (Nicotiana benthamiana) Pseudomonas fluorescens

Heterologous gene encoding siderophore responsible for iron uptake pTOM toluenedegradation plasmid Cf-4 (Fungal gene)

–

Bacillus sp.

Burkholderia cepacia G4 Wild tomato

Effect Virus resistant plants Improved root architect and plant protection

Reference Azad et al. (2014) Wang et al. (2000)

Protect from plant pathogen Pectobacterium Phytoremediation

Dong et al. (2000)

Canker resistance and defence

Savka et al. (2002) Hao et al. (2016)

Improved the competitiveness in soil

Raaijmakers et al. (1995)

Phytoremediation

Barac et al. (2004) Oliver et al. (2000)

Resistance to the fungal tomato pathogen Cladosporium fulvum

and improving the capacity of agricultural crops to extract water from the soil are the main research objectives. To increase water efficiency in crop production, many advocate the use of genetic modification. Genetically modified crops, however, may have unforeseen evolutionary repercussions for ecosystems. Another potential technique used by plants to maximise water absorption is to change the rhizosphere, the atmosphere in which the roots grow and interact with them (York et al. 2016). The presence of mucilage, a polymeric gel that exudes from most plant roots, is of particular interest. Recent studies have drawn attention to the role of mucilage in forming hydraulic properties in the rhizosphere and controlling the absorption of root water. The mucilage keeps the rhizosphere moist and conductive during drying, but it becomes hydrophobic upon drying, restricting the absorption of root water. Ahmed et al. (2018) used the concept of rhizoligands, defined as additives that (i) rewet the rhizosphere and (ii) decrease mucilage swelling, thus reducing the conductivity of the rhizosphere. They stated that the interaction between rhizoligands and the mucilage exuded by roots caused a decrease in transpiration in Lupinus albus. Rolli et al. (2015) reported that Acinetobacter sp. S2 and Bacillus

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Fig. 25.3 Benefits of rhizosphere engineering in horticultural crops

sp. S4, Sphingobacterium sp. S6, Enterobacter sp. S7 and Delftia sp. S8 enhanced drought tolerance in Capsicum annuum, as well as increased fresh root, aerial biomass and photosynthesis. Nordstedt et al. (2020) identified two Pseudomonads, P. poae 29G9 and P. fluorescens 90F12–2, that enhance the quality of three ornamental plants, that is, Petunia  hybrida, Impatiens walleriana, and Viola  wittrockiana, under drought conditions.

25.7.2 Disease Resistance In general, bacterial and fungal pathogens are a significant threat to sustainability, quality and yield of horticultural crops. Therefore, growers follow various practices such as proper sanitation of the planting fields, crop rotation, use of disease-resistant cultivars and indiscriminate use of chemicals to minimise the yield losses caused by phytopathogens and therefore to maximise vegetable output. Despite following too many tactics, including the excessive use of chemicals, significant success in combating plant diseases has not been achieved in horticultural production. Therefore, to boost production and to increase the yield by minimising the losses due to pathogen attacks, in recent times, emphasis has been shifted towards the use of cheap, eco-friendly and viable alternatives such as PGPR in the management of plant diseases to minimise yield losses therefrom. This has significantly increased the growth, yield and quality of many vegetables due to the application of PGPR. Shanthiyaa et al. (2013) reported that late blight of potato can be effectively controlled by applying PGPR, that is, Chaetomium globosum; Burkholderia cepacia. Pseudomonas spp. isolated from pea, wheat, cotton, tomato, sugarbeet

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and tobacco reduced disease severity and abundance of Ralstonia solanacearum in tomato plants (Hu et al. 2016). Jayapala et al. (2019) stated that rhizobacteria Bacillus spp. induce resistance against anthracnose disease in chilli by activating host defence response.

25.7.3 Rhizoremediation An emerging field of interest is the use of plants and microbes for the rehabilitation of heavy-metal-contaminated habitats because they provide an ecologically sustainable and healthy approach for restoration and remediation. Wu et al. (2006) showed that the expression of a metal-binding peptide (EC20) in Pseudomonas putida 06909, a rhizobacterium, not only strengthened cadmium binding, but also alleviated cadmium cell toxicity. More significantly, inoculation of the sunflower roots with the engineered rhizobacterium resulted in a substantial decrease in the phytotoxicity of cadmium and a 40 percent increase in the accumulation of cadmium in the plant roots. The use of EC20-expressing P. putida with organic-degrading capabilities could be a promising strategy for remediating mixed organic-metal-contaminated sites due to the significantly improved growth characteristics of both the rhizobacterium and the plant. Wang et al. (2020) screened bacterial population for heavy metal resistance Its effect on reducing Cd2+ and Pb2+ concentrations in water spinach (Ipomoea aquatic Forsk.) and reported three heavy metal-immobilising bacteria, Enterobacter bugandensis CQ-7, Bacillus thuringensis CQ-33 and Klebsiella michiganensis CQ-169 produced siderophores and IAA and were highly resistant to Cd2+ and Pb2+. The results showed that heavy metal-immobilising bacteria played significant role in vegetable growth and accumulation of metals. The findings also highlighted that the efficacy of heavy metal-immobilising bacteria-vegetable systems must be checked and experimental designs should be developed in managed vegetation, taking into account the precise matching of vegetables and bacteria.

25.7.4 Regulation of Flowering It was found that microbial communities in the rhizosphere could modulate the timing of Arabidopsis thaliana flowering. By converting tryptophan to the phytohormone indole acetic acid (IAA), rhizosphere microorganisms that increased and prolonged N bioavailability via nitrification delayed flowering, thereby downregulating genes that cause flowering, and stimulating further plant development (Lu et al. 2018). Manipulation of flowering time through microbial community is a very good approach which will help the horticulturist produce crops during the off-season.

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25.7.5 Rooting of Cuttings Most of the fruits and floriculture crops are being propagated by vegetative means. PGPR play a very important role in the rooting of plants. To obtain organic nursery material, the use of PGPR for the multiplication of nursery material may be necessary because the use of all formulations of synthetic plant growth regulators such as indole-3-butyric acid (IBA) are banned worldwide. In addition, the success of root promotion depends on the strain and genotypic response of the plant species used. Erturk et al. (2010) studied the effect of PGPR (Bacillus RC23, Paenibacillus polymyxa RC05, Bacillus subtilis OSU142, Bacillus RC03, Comamonas acidovorans RC41, Bacillus megaterium RC01 and Bacillus simplex RC19) on rooting of cuttings of Kiwifruit and revealed that the highest rooting ratios were obtained when the cuttings were treated with Bacillus spp. Sezen et al. (2014) reported that inoculations with PGPR stimulate adventitious root formation on semi-hardwood stem cuttings of Ficus benjamina. Researchers reported that Bacillus subtilus (BA-142) may possess great potential for promoting adventitious root formation in Ficus benjamina. The abovementioned finding suggests that PGPR can be used in the organic production of nursery material.

25.8

Conclusion

Numerous microbial inoculants have been established due to the high potential of microorganisms to enhance plant development, stress tolerance and health, but many of them show poor performance in the field. Several approaches can contribute to improved field performance, such as the design of the able microbial consortia, the selection of agricultural management practices that favour beneficial microbiota or a new generation of approaches to plant breeding. Various studies have shown that the rhizosphere can be engineered by selecting the right crop species and varieties, by adding microorganisms or soil alterations, and by manipulating plant and microbial processes genetically. The development of molecular technology now allows for the direct alteration of genes that influence rhizosphere functions. Biotechnology would ensure more progress in the future. Our capacity to alter the rhizosphere efficiently and predictably remains a problem, despite encouraging improvements in a variety of areas. It is important for the scientists to continue their work so that the public can be benefitted from secure, sustainable and environment-friendly agricultural practices. Acknowledgement Authors acknowledge the Director, CSIR-Institute of Himalayan Bioresource Technology, Palampur, for supporting and providing all the necessary facilities. This manuscript represents CSIR-IHBT communication number: 4935. Conflict of Interest Authors declare no conflict of interest.

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